Strength and Conditioning
Biological Principles and Practical Applications
Edited by
Marco Cardinale, Rob Newton and Kazunori Nosaka
A John Wiley & Sons, Ltd., Publication
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Strength and Conditioning
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Strength and Conditioning
Biological Principles and Practical Applications
Edited by
Marco Cardinale, Rob Newton and Kazunori Nosaka
A John Wiley & Sons, Ltd., Publication
ffirs.indd iii
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This edition first published 2011 © 2011, John Wiley & Sons, Ltd.
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Library of Congress Cataloguing-in-Publication Data
Strength and conditioning – biological principles and practical applications / edited by Marco Cardinale, Rob
Newton, and Kazunori Nosaka.
p. ; cm.
Includes bibliographical references and index.
ISBN 978-0-470-01918-4 (cloth) – ISBN 978-0-470-01919-1 (pbk.)
1. Muscle strength. 2. Exercise–Physiological aspects. 3. Physical education and training. I. Cardinale,
Marco. II. Newton, Rob (Robert U.) III. Nosaka, Kazunori.
[DNLM: 1. Physical Fitness. 2. Exercise. 3. Physical Endurance. QT 255]
QP321.S885 2011
613.7′11–dc22
2010029179
A catalogue record for this book is available from the British Library.
This book is published in the following electronic format: ePDF 9780470970003
Set in 9 on 10.5pt Times by Toppan Best-set Premedia Limited
First Impression 2011
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Contents
Foreword by Sir Clive Woodward
Preface
List of Contributors
1.2.3.3 Surface EMG for noninvasive
neuromuscular assessment
xiii
xv
xvii
1.3
Section 1 Strength and Conditioning
Biology
1.1 Skeletal Muscle Physiology
Valmor Tricoli
1.1.1 Introduction
1.1.2 Skeletal Muscle Macrostructure
1.1.3 Skeletal Muscle Microstructure
1.1.3.1 Sarcomere and myofilaments
1.1.3.2 Sarcoplasmic reticulum and
transverse tubules
1.1.4 Contraction Mechanism
1.1.4.1 Excitation–contraction (E-C)
coupling
1.1.4.2 Skeletal muscle contraction
1.1.5 Muscle Fibre Types
1.1.6 Muscle Architecture
1.1.7 Hypertrophy and Hyperplasia
1.1.8 Satellite Cells
1.2
ftoc.indd v
1
3
3
3
3
4
7
7
7
7
9
10
11
12
Neuromuscular Physiology
Alberto Rainoldi and Marco Gazzoni
17
1.2.1 The Neuromuscular System
1.2.1.1 Motor units
1.2.1.2 Muscle receptors
1.2.1.3 Nervous and muscular conduction
velocity
1.2.1.4 Mechanical output production
1.2.1.5 Muscle force modulation
1.2.1.6 Electrically elicited contractions
1.2.2 Muscle Fatigue
1.2.2.1 Central and peripheral fatigue
1.2.2.2 The role of oxygen availability
in fatigue development
1.2.3 Muscle Function Assessment
1.2.3.1 Imaging techniques
1.2.3.2 Surface EMG as a muscle imaging
tool
17
17
17
18
18
20
22
22
22
23
23
23
24
Bone Physiology
Jörn Rittweger
1.3.1 Introduction
1.3.2 Bone Anatomy
1.3.2.1 Bones as organs
1.3.2.2 Bone tissue
1.3.2.3 The material level: organic
and inorganic constituents
1.3.3 Bone Biology
1.3.3.1 Osteoclasts
1.3.3.2 Osteoblasts
1.3.3.3 Osteocytes
1.3.4 Mechanical Functions of Bone
1.3.4.1 Material properties
1.3.4.2 Structural properties
1.3.5 Adaptive Processes in Bone
1.3.5.1 Modelling
1.3.5.2 Remodelling
1.3.5.3 Theories of bone adaptation
1.3.5.4 Mechanotransduction
1.3.6 Endocrine Involvement of Bone
1.3.6.1 Calcium homoeostasis
1.3.6.2 Phosphorus homoeostasis
1.3.6.3 Oestrogens
1.4
25
29
29
29
29
30
31
32
32
32
33
33
33
34
35
35
35
36
37
38
38
38
38
Tendon Physiology
45
Nicola Maffulli, Umile Giuseppe Longo,
Filippo Spiezia and Vincenzo Denaro
1.4.1
1.4.2
1.4.3
1.4.4
1.4.5
1.4.6
1.4.7
1.4.8
1.4.9
1.4.10
Tendons
The Musculotendinous Junction
The Oseotendinous Junction
Nerve Supply
Blood Supply
Composition
Collagen Formation
Cross-Links
Elastin
Cells
45
46
46
46
46
47
47
47
48
48
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vi
CONTENTS
1.4.11
1.4.12
Ground Substance
Crimp
1.5 Bioenergetics of Exercise
Ron J. Maughan
1.5.1 Introduction
1.5.2 Exercise, Energy, Work, and Power
1.5.3 Sources of Energy
1.5.3.1 Phosphagen metabolism
1.5.3.2 The glycolytic system
1.5.3.3 Aerobic metabolism: oxidation
of carbohydrate, lipid, and protein
1.5.4 The Tricarboxylic Acid (TCA) Cycle
1.5.5 Oxygen Delivery
1.5.6 Energy Stores
1.5.7 Conclusion
1.6 Respiratory and Cardiovascular
Physiology
Jeremiah J. Peiffer and Chris R. Abbiss
1.6.1 The Respiratory System
1.6.1.1 Introduction
1.6.1.2 Anatomy
1.6.1.3 Gas exchange
1.6.1.4 Mechanics of ventilation
1.6.1.5 Minute ventilation
1.6.1.6 Control of ventilation
1.6.2 The Cardiovascular System
1.6.2.1 Introduction
1.6.2.2 Anatomy
1.6.2.3 The heart
1.6.2.4 The vascular system
1.6.2.5 Blood and haemodynamics
1.6.3 Conclusion
1.7
1.7.2.6 Signalling associated with muscle
protein breakdown
1.7.2.7 Satellite-cell regulation during
strength training
1.7.2.8 What we have not covered
53
53
53
54
55
56
57
57
58
58
60
63
63
63
63
63
66
67
68
68
68
68
70
71
72
74
Genetic and Signal Transduction
Aspects of Strength Training
77
Henning Wackerhage, Arimantas Lionikas,
Stuart Gray and Aivaras Ratkevicius
1.7.1 Genetics of Strength and Trainability
1.7.1.1 Introduction to sport and exercise
genetics
1.7.1.2 Heritability of muscle mass,
strength, and strength trainability
1.7.2 Signal Transduction Pathways that
Mediate the Adaptation to Strength
Training
1.7.2.1 Introduction to adaptation to
exercise: signal transduction
pathway regulation
1.7.2.2 Human protein synthesis and
breakdown after exercise
1.7.2.3 The AMPK–mTOR system and the
regulation of protein synthesis
1.7.2.4 Potential practical implications
1.7.2.5 Myostatin–Smad signalling
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48
48
77
77
77
79
79
80
81
82
83
1.8
Strength and Conditioning
Biomechanics
Robert U. Newton
83
84
84
89
1.8.1 Introduction
89
1.8.1.1 Biomechanics and sport
89
1.8.2 Biomechanical Concepts for Strength
and Conditioning
89
1.8.2.1 Time, distance, velocity, and
acceleration
90
1.8.2.2 Mass, force, gravity, momentum,
work, and power
90
1.8.2.3 Friction
91
1.8.3 The Force–Velocity–Power Relationship 91
1.8.4 Musculoskeletal Machines
92
1.8.4.1 Lever systems
92
1.8.4.2 Wheel-axle systems
93
1.8.5 Biomechanics of Muscle Function
93
1.8.5.1 Length–tension effect
93
1.8.5.2 Muscle angle of pull
93
1.8.5.3 Strength curve
94
1.8.5.4 Line and magnitude of resistance
95
1.8.5.5 Sticking region
95
1.8.5.6 Muscle architecture, strength,
and power
95
1.8.5.7 Multiarticulate muscles, active
and passive insufficiency
96
1.8.6 Body Size, Shape, and Power-ToWeight Ratio
96
1.8.7 Balance and Stability
96
1.8.7.1 Factors contributing to stability
96
1.8.7.2 Initiating movement or change
of motion
97
1.8.8 The Stretch–Shortening Cycle
97
1.8.9 Biomechanics of Resistance
Machines
98
1.8.9.1 Free weights
98
1.8.9.2 Gravity-based machines
98
1.8.9.3 Hydraulic resistance
99
1.8.9.4 Pneumatic resistance
99
1.8.9.5 Elastic resistance
100
1.8.10 Machines vs Free Weights
100
1.8.11 Conclusion
100
Section 2 Physiological adaptations to
strength and conditioning
2.1 Neural Adaptations to Resistance
Exercise
Per Aagaard
2.1.1 Introduction
2.1.2 Effects of Strength Training on
Mechanical Muscle Function
103
105
105
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CONTENTS
2.1.2.1 Maximal concentric and eccentric
muscle strength
2.1.2.2 Muscle power
2.1.2.3 Contractile rate of force
development
2.1.3 Effects of Strength Training on
Neural Function
2.1.3.1 Maximal EMG amplitude
2.1.3.2 Contractile RFD: changes in
neural factors with strength
training
2.1.3.3 Maximal eccentric muscle
contraction: changes in neural
factors with strength training
2.1.3.4 Evoked spinal motor neuron
responses
2.1.3.5 Excitability in descending
corticospinal pathways
2.1.3.6 Antagonist muscle coactivation
2.1.3.7 Force steadiness, fine motor
control
2.1.4 Conclusion
2.2 Structural and Molecular Adaptations
to Training
Jesper L. Andersen
2.2.1 Introduction
2.2.2 Protein Synthesis and Degradation
in Human Skeletal Muscle
2.2.3 Muscle Hypertrophy and Atrophy
2.2.3.1 Changes in fibre type composition
with strength training
2.2.4 What is the Significance of Satellite
Cells in Human Skeletal Muscle?
2.2.5 Concurrent Strength and Endurance
Training: Consequences for Muscle
Adaptations
2.3 Adaptive Processes in Human Bone
and Tendon
Constantinos N. Maganaris, Jörn
Rittweger and Marco V. Narici
2.3.1 Introduction
2.3.2 Bone
2.3.2.1 Origin of musculoskeletal forces
2.3.2.2 Effects of immobilization on
bone
2.3.2.3 Effects of exercise on bone
2.3.2.4 Bone adaptation across the
life span
2.3.3 Tendon
2.3.3.1 Functional and mechanical
properties
2.3.3.2 In vivo testing
2.3.3.3 Tendon adaptations to altered
mechanical loading
2.3.4 Conclusion
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106
107
107
108
109
110
114
116
116
119
119
125
2.4 Biochemical Markers and Resistance
Training
Christian Cook and Blair Crewther
vii
155
2.4.1 Introduction
2.4.2 Testosterone Responses to Resistance
Training
2.4.2.1 Effects of workout design
2.4.2.2 Effects of age and gender
2.4.2.3 Effects of training history
2.4.3 Cortisol Responses to Resistance
Training
2.4.3.1 Effects of workout design
2.4.3.2 Effects of age and gender
2.4.3.3 Effects of training history
2.4.4 Dual Actions of Testosterone and
Cortisol
2.4.5 Growth Hormone Responses to
Resistance Training
2.4.5.1 Effects of workout design
2.4.5.2 Effects of age and gender
2.4.5.3 Effects of training history
2.4.6 Other Biochemical Markers
2.4.7 Limitations in the Use and
Interpretation of Biochemical Markers
2.4.8 Applications of Resistance Training
2.4.9 Conclusion
155
155
155
156
156
156
156
157
157
157
157
158
158
158
158
159
159
160
125
2.5
125
127
128
131
132
137
137
137
137
138
140
140
141
141
143
143
147
Cardiovascular Adaptations to
Strength and Conditioning
165
Andrew M. Jones and Fred J. DiMenna
2.5.1 Introduction
2.5.2 Cardiovascular Function
2.5.2.1 Oxygen uptake
2.5.2.2 Maximal oxygen uptake
2.5.2.3 Cardiac output
2.5.2.4 Cardiovascular overload
2.5.2.5 The cardiovascular training
stimulus
2.5.2.6 Endurance exercise training
2.5.3 Cardiovascular Adaptations to Training
2.5.3.1 Myocardial adaptations to
endurance training
2.5.3.2 Circulatory adaptations to
endurance training
2.5.4 Cardiovascular-Related Adaptations
to Training
2.5.4.1 The pulmonary system
2.5.4.2 The skeletal muscular system
2.5.5 Conclusion
2.6 Exercise-induced Muscle Damage
and Delayed-onset Muscle Soreness
(DOMS)
Kazunori Nosaka
2.6.1 Introduction
2.6.2 Symptoms and Markers of
Muscle Damage
165
165
165
165
165
166
167
167
167
167
170
172
172
173
174
179
179
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viii
CONTENTS
2.6.2.1 Symptoms
2.6.2.2 Histology
2.6.2.3 MRI and B-mode ultrasound
images
2.6.2.4 Blood markers
2.6.2.5 Muscle function
2.6.2.6 Exercise economy
2.6.2.7 Range of motion (ROM)
2.6.2.8 Swelling
2.6.2.9 Muscle pain
2.6.3 Relationship between Doms and
Other Indicators
2.6.4 Factors Influencing the Magnitude
of Muscle Damage
2.6.4.1 Contraction parameters
2.6.4.2 Training status
2.6.4.3 Repeated-bout effect
2.6.4.4 Muscle
2.6.4.5 Other factors
2.6.5 Muscle Damage and Training
2.6.5.1 The importance of eccentric
contractions
2.6.5.2 The possible role of muscle
damage in muscle hypertrophy
and strength gain
2.6.5.3 No pain, no gain?
2.6.6 Conclusion
2.7 Alternative Modalities of Strength
and Conditioning: Electrical
Stimulation and Vibration
Nicola A. Maffiuletti and Marco
Cardinale
2.7.1 Introduction
2.7.2 Electrical-Stimulation Exercise
2.7.2.1 Methodological aspects: ES
parameters and settings
2.7.2.2 Physiological aspects: motor unit
recruitment and muscle fatigue
2.7.2.3 Does ES training improve muscle
strength?
2.7.2.4 Could ES training improve sport
performance?
2.7.2.5 Practical suggestions for ES use
2.7.3 Vibration Exercise
2.7.3.1 Is vibration a natural stimulus?
2.7.3.2 Vibration training is not just
about vibrating platforms
2.7.3.3 Acute effects of vibration in
athletes
2.7.3.4 Acute effects of vibration
exercise in non-athletes
2.7.3.5 Chronic programmes of vibration
training in athletes
2.7.3.6 Chronic programmes of vibration
training in non-athletes
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179
2.7.3.7 Applications in rehabilitation
2.7.3.8 Safety considerations
203
203
180
180
181
182
182
182
183
2.8 The Stretch–Shortening Cycle (SSC)
Anthony Blazevich
209
2.8.1 Introduction
2.8.2 Mechanisms Responsible for
Performance Enhancement with
the SSC
2.8.2.1 Elastic mechanisms
2.8.2.2 Contractile mechanisms
2.8.2.3 Summary of mechanisms
2.8.3 Force Unloading: A Requirement
for Elastic Recoil
2.8.4 Optimum MTU Properties for SSC
Performance
2.8.5 Effects of the Transition Time
between Stretch and Shortening
on SSC Performance
2.8.6 Conclusion
209
184
184
185
185
185
186
186
187
187
187
188
188
193
193
193
193
194
195
196
196
197
200
201
201
202
202
203
209
209
212
216
216
217
218
218
2.9 Repeated-sprint Ability (RSA)
David Bishop and Olivier Girard
223
2.9.1 Introduction
2.9.1.1 Definitions
2.9.1.2 Indices of RSA
2.9.2 Limiting Factors
2.9.2.1 Muscular factors
2.9.2.2 Neuromechanical factors
2.9.2.3 Summary
2.9.3 Ergogenic aids and RSA
2.9.3.1 Creatine
2.9.3.2 Carbohydrates
2.9.3.3 Alkalizing agents
2.9.3.4 Caffeine
2.9.3.5 Summary
2.9.4 Effects of Training on RSA
2.9.4.1 Introduction
2.9.4.2 Training the limiting factors
2.9.4.3 Putting it all together
2.9.5 Conclusion
223
223
223
223
224
227
229
229
230
230
230
231
232
232
232
232
235
235
2.10 The Overtraining Syndrome (OTS)
Romain Meeusen and Kevin De Pauw
243
2.10.1 Introduction
2.10.2 Definitions
2.10.2.1 Functional overreaching (FO)
2.10.2.2 Nonfunctional overreaching
(NFO)
2.10.2.3 The overtraining syndrome
(OTS)
2.10.2.4 Summary
2.10.3 Prevalence
2.10.4 Mechanisms and Diagnosis
2.10.4.1 Hypothetical mechanisms
2.10.4.2 Biochemistry
243
243
243
244
244
244
244
245
245
245
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CONTENTS
2.10.4.3 Physiology
2.10.4.4 The immune system
2.10.4.5 Hormones
2.10.4.6 Is the brain involved?
2.10.4.7 Training status
2.10.4.8 Psychometric measures
2.10.4.9 Psychomotor speed
2.10.4.10 Are there definitive
diagnostic criteria?
2.10.5 Prevention
2.10.6 Conclusion
Section 3 Monitoring strength and
conditioning progress
3.1 Principles of Athlete Testing
Robert U. Newton, Prue Cormie and
Marco Cardinale
3.1.1 Introduction
3.1.2 General Principles of Testing
Athletes
3.1.2.1 Validity
3.1.2.2 Reliability
3.1.2.3 Specificity
3.1.2.4 Scheduling
3.1.2.5 Selection of movement tested
3.1.2.6 Stretching and other preparation
for the test
3.1.3 Maximum Strength
3.1.3.1 Isoinertial strength testing
3.1.3.2 Isometric strength testing
3.1.3.3 Isokinetic strength testing
3.1.4 Ballistic Testing
3.1.4.1 Jump squats
3.1.4.2 Rate of force development
(RFD)
3.1.4.3 Temporal phase analysis
3.1.4.4 Equipment and analysis methods
for ballistic testing
3.1.5 Reactive Strength Tests
3.1.6 Eccentric Strength Tests
3.1.6.1 Specific tests of skill
performance
3.1.6.2 Relative or absolute measures
3.1.7 Conclusion
245
246
246
246
247
247
247
248
248
249
253
255
3.3.1 Introduction
3.3.1.1 Energy systems
3.3.1.2 The importance of anaerobic
capacity and RSA
3.3.2 Testing Anaerobic Capacity
3.3.2.1 Definition
3.3.2.2 Assessment
3.3.3 Testing Repeated-Sprint Ability
3.3.3.1 Definition
3.3.3.2 Assessment
3.3.4 Conclusion
3.4
255
255
255
255
255
256
256
256
257
257
258
259
259
260
261
261
264
265
266
267
267
267
3.2 Speed and Agility Assessment
Warren Young and Jeremy Sheppard
271
3.2.1 Speed
3.2.1.1 Introduction
3.2.1.2 Testing acceleration speed
3.2.1.3 Testing maximum speed
3.2.1.4 Testing speed endurance
3.2.1.5 Standardizing speed-testing
protocols
3.2.2 Agility
3.2.3 Conclusion
271
271
271
272
272
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3.3 Testing Anaerobic Capacity and
Repeated-sprint Ability
David Bishop and Matt Spencer
273
273
275
ix
277
277
277
277
277
277
279
284
284
284
286
Cardiovascular Assessment and
Aerobic Training Prescription
291
Andrew M. Jones and Fred J. DiMenna
3.4.1 Introduction
3.4.2 Cardiovascular Assessment
3.4.2.1 Health screening and risk
stratification
3.4.2.2 Cardiorespiratory fitness
and VO2max
3.4.2.3 Submaximal exercise testing
3.4.2.4 Maximal exercise testing
3.4.3 Aerobic Training Prescription
3.4.3.1 Specificity and aerobic overload
3.4.3.2 Mode
3.4.3.3 Frequency
3.4.3.4 Total volume
3.4.3.5 Intensity
3.4.3.6 Total volume vs volume per
unit time
3.4.3.7 Progression
3.4.3.8 Reversibility
3.4.3.9 Parameter-specific
cardiorespiratory enhancement
3.4.3.10 VO2max improvement
3.4.3.11 Exercise economy improvement
3.4.3.12 LT/LTP improvement
3.4.3.13 VO2 kinetics improvement
3.4.3.14 Prescribing exercise for
competitive athletes
3.4.4 Conclusion
3.5 Biochemical Monitoring in Strength
and Conditioning
Michael R. McGuigan and Stuart J.
Cormack
3.5.1 Introduction
3.5.2 Hormonal Monitoring
3.5.2.1 Cortisol
3.5.2.2 Testosterone
3.5.2.3 Catecholamines
3.5.2.4 Growth hormone
291
291
291
291
292
292
297
297
297
297
298
298
298
299
299
299
299
300
300
300
301
301
305
305
305
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CONTENTS
3.5.2.5 IGF
306
3.5.2.6 Leptin
307
3.5.2.7 Research on hormones in sporting
environments
307
3.5.2.8 Methodological considerations
308
3.5.3 Metabolic Monitoring
308
3.5.3.1 Muscle biopsy
308
3.5.3.2 Biochemical testing
309
3.5.4 Immunological and Haematological
Monitoring
309
3.5.4.1 Immunological markers
309
3.5.4.2 Haematological markers
310
3.5.5 Practical Application
310
3.5.5.1 Evaluating the effects of training 310
3.5.5.2 Assessment of training workload 311
3.5.5.3 Monitoring of fatigue
311
3.5.5.4 Conclusions and specific advice for
implementation of a biochemical
monitoring programme
311
3.6 Body Composition: Laboratory and
Field Methods of Assessment
Arthur Stewart and Tim Ackland
3.6.1 Introduction
3.6.2 History of Body Composition
Methods
3.6.3 Fractionation Models for Body
Composition
3.6.4 Biomechanical Imperatives for Sports
Performance
3.6.5 Methods of Assessment
3.6.5.1 Laboratory methods
3.6.5.2 Field methods
3.6.6 Profiling
3.6.7 Conclusion
317
317
317
317
318
319
319
323
330
330
3.7 Total Athlete Management (TAM)
and Performance Diagnosis
335
Robert U. Newton and Marco Cardinale
3.7.1 Total Athlete Management
335
3.7.1.1 Strength and conditioning
335
3.7.1.2 Nutrition
335
3.7.1.3 Rest and recovery
336
3.7.1.4 Travel
336
3.7.2 Performance Diagnosis
336
3.7.2.1 Optimizing training-programme
design and the window of
adaptation
337
3.7.2.2 Determination of key performance
characteristics
338
3.7.2.3 Testing for specific performance
qualities
339
3.7.2.4 What to look for
339
3.7.2.5 Assessing imbalances
339
3.7.2.6 Session rating of
perceived exertion
340
ftoc.indd x
3.7.2.7 Presenting the results
3.7.2.8 Sophisticated is not necessarily
expensive
3.7.2.9 Recent advances and the future
3.7.3 Conclusion
340
340
341
342
Section 4 Practical applications
4.1 Resistance Training Modes:
A Practical Perspective
Michael H. Stone and Margaret
E. Stone
345
347
4.1.1 Introduction
4.1.2 Basic Training Principles
4.1.2.1 Overload
4.1.2.2 Variation
4.1.2.3 Specificity
4.1.3 Strength, Explosive Strength,
and Power
4.1.3.1 Joint-angle specificity
4.1.3.2 Movement-pattern specificity
4.1.3.3 Machines vs free weights
4.1.3.4 Practical considerations:
advantages and disadvantages
associated with different
modes of training
4.1.4 Conclusion
347
348
348
348
348
348
349
350
351
355
357
4.2 Training Agility and Change-ofdirection Speed (CODS)
Jeremy Sheppard and Warren Young
4.2.1 Factors Affecting Agility
4.2.2 Organization of Training
4.2.3 Change-of-Direction Speed
4.2.3.1 Leg-strength qualities and CODS
4.2.3.2 Technique
4.2.3.3 Anthropometrics and CODS
4.2.4 Perceptual and Decision-Making
Factors
4.2.5 Training Agility
4.2.6 Conclusion
4.3 Nutrition for Strength Training
Christopher S. Shaw and
Kevin D. Tipton
4.3.1 Introduction
4.3.2 The Metabolic Basis of Muscle
Hypertrophy
4.3.3 Optimal Protein Intake
4.3.3.1 The importance of energy
balance
4.3.4 Acute Effects of Amino Acid/Protein
Ingestion
4.3.4.1 Amino acid source
4.3.4.2 Timing
4.3.4.3 Dose
4.3.4.4 Co-ingestion of other nutrients
363
363
363
364
366
366
369
370
371
374
377
377
377
377
378
379
379
381
382
382
10/19/2010 10:00:57 AM
CONTENTS
4.3.4.5 Protein supplements
4.3.4.6 Other supplements
4.3.5 Conclusion
4.4
Flexibility
William A. Sands
4.4.1 Definitions
4.4.2 What is Stretching?
4.4.3 A Model of Effective Movement: The
Integration of Flexibility and Strength
4.5
5.1.3.5 Training of sport-specific
movements
5.1.4 Conclusion
389
5.2 Strength Training for Children
and Adolescents
Avery D. Faigenbaum
389
390
393
Sensorimotor Training
399
Urs Granacher, Thomas Muehlbauer,
Wolfgang Taube, Albert Gollhofer and
Markus Gruber
4.5.1 Introduction
4.5.2 The Importance of Sensorimotor
Training to the Promotion of Postural
Control and Strength
4.5.3 The Effects of Sensorimotor Training
on Postural Control and Strength
4.5.3.1 Sensorimotor training in healthy
children and adolescents
4.5.3.2 Sensorimotor training in healthy
adults
4.5.3.3 Sensorimotor training in healthy
seniors
4.5.4 Adaptive Processes Following
Sensorimotor Training
4.5.5 Characteristics of Sensorimotor
Training
4.5.5.1 Activities
4.5.5.2 Load dimensions
4.5.5.3 Supervision
4.5.5.4 Efficiency
4.5.6 Conclusion
Section 5 Strength and Conditioning
special cases
5.1 Strength and Conditioning as a
Rehabilitation Tool
Andreas Schlumberger
5.1.1 Introduction
5.1.2 Neuromuscular Effects of Injury as
a Basis for Rehabilitation Strategies
5.1.3 Strength and Conditioning in
Retraining of the Neuromuscular
System
5.1.3.1 Targeted muscle overloading:
criteria for exercise choice
5.1.3.2 Active lengthening/eccentric
training
5.1.3.3 Passive lengthening/stretching
5.1.3.4 Training of the muscles of the
lumbopelvic hip complex
ftoc.indd xi
383
383
383
399
400
401
401
401
401
402
402
402
403
405
405
406
411
413
413
414
415
415
417
419
421
5.2.1 Introduction
5.2.2 Risks and Concerns Associated with
Youth Strength Training
5.2.3 The Effectiveness of Youth
Resistance Training
5.2.3.1 Persistence of training-induced
strength gains
5.2.3.2 Programme evaluation
and testing
5.2.4 Physiological Mechanisms for
Strength Development
5.2.5 Potential Health and Fitness Benefits
5.2.5.1 Cardiovascular risk profile
5.2.5.2 Bone health
5.2.5.3 Motor performance skills and
sports performance
5.2.5.4 Sports-related injuries
5.2.6 Youth Strength-Training Guidelines
5.2.6.1 Choice and order of exercise
5.2.6.2 Training intensity and volume
5.2.6.3 Rest intervals between sets
and exercises
5.2.6.4 Repetition velocity
5.2.6.5 Training frequency
5.2.6.6 Programme variation
5.2.7 Conclusion
Acknowledgements
5.3
Strength and Conditioning
Considerations for the Paralympic
Athlete
Mark Jarvis, Matthew Cook and
Paul Davies
5.3.1 Introduction
5.3.2 Programming Considerations
5.3.3 Current Controversies in Paralympic
Strength and Conditioning
5.3.4 Specialist Equipment
5.3.5 Considerations for Specific
Disability Groups
5.3.5.1 Spinal-cord injuries
5.3.5.2 Amputees
5.3.5.3 Cerebral palsy
5.3.5.4 Visual impairment
5.3.5.5 Intellectual disabilities
5.3.5.6 Les autres
5.3.6 Tips for More Effective Programming
Index
xi
422
423
427
427
427
429
429
429
430
430
431
431
432
432
432
433
434
434
435
435
435
435
435
441
441
441
442
443
443
443
445
446
447
448
449
449
453
10/19/2010 10:00:57 AM
ftoc.indd xii
10/19/2010 10:00:57 AM
Foreword by Sir Clive Woodward
High-level performance may seem easy to sport fans. Coaches
and athletes know very well that it is very difficult to achieve.
Winning does not happen in a straight line. It is the result of
incredible efforts, dedication, passion, but also the result of the
willingness to learn something new every day in every possible
field which can help improve performance.
Strength and conditioning is fundamental for preparing athletes to perform at their best. It is also important to provide
better quality of life in special populations and improve fitness.
Scientific efforts in this field have improved enormously our
understanding of various training methods and nutritional interventions to maximize performance. Furthermore, due to the
advancement in technology, we are nowadays capable of measuring in real time many things able to inform the coach on the
best way to improve the quality of the training programmes.
Winning the World Cup in 2003 was a great achievement.
And in my view the quality of our strength and conditioning
programme was second to none thanks to the ability of our staff
to translate the latest scientific knowledge into innovative practical applications. The success of Team GB in Beijing has also
been influenced by the continuous advancement of the strength
and conditioning profession in the UK as well as the ability of
our practitioners to continue their quest for knowledge in this
fascinating field.
Now, even better and more information is available to
coaches, athletes, sports scientists and sports medicine professionals willing to learn more about the field of strength and
conditioning. Strength and Conditioning: Biological Principles
and Practical Applications is a must read for everyone serious
about this field. The editors, Dr Marco Cardinale, Dr Robert
fbetw.indd xiii
Newton and Dr Kazunori Nosaka are world leaders in this field
and have collected an outstanding list of authors for all the
chapters. Great scientists have produced an incredible resource
to provide the reader with all the details needed to understand
more about the biology of strength and conditioning and the
guidance to pick the appropriate applications when designing
training programmes.
When a group of sports scientific leaders from all over the
world come together to produce a book about the human body
and performance, the reader can be assured the material is at
the leading edge of sports science. Success in sport is nowadays
the result of a word class coach working with a world class
athlete surrounded by the best experts possible in various fields.
This does not mean the coach needs to delegate knowledge to
others. A modern coach must be aware of the science to be able
to challenge his/her support team and always stimulate the quest
for best practice and innovation.
The book contains the latest information on many subjects
including overtraining, muscle structure and function and its
adaptive changes with training, hormonal regulation, nutrition,
testing and training planning modalities, and most of all it
provides guidance for the appropriate use of strength and conditioning with young athletes, paralympians and special
populations.
I recommend that you read and use the information in this
book to provide your athletes with the best chances of performing at their best.
Sir Clive Woodward
Director of Sport
British Olympic Association
10/18/2010 5:12:10 PM
fbetw.indd xiv
10/18/2010 5:12:10 PM
Preface
In order to optimise athletic performance, athletes must be
optimally trained. The science of training has evolved enormously in the last twenty years as a direct result of the large
volume of research conducted on specific aspects and thanks to
the development of innovative technology capable of measuring athletic performance in the lab and directly onto the field.
Strength and conditioning is now a well recognised profession
in many countries and professional organisations as well as
academic institutions strive to educate in the best possible way
strength and conditioning experts able to work not only with
elite sports people but also with the general population. Strength
and conditioning is now acknowledged as a critical component
in the development and management of the elite athlete as well
as broad application of the health and fitness regime of the
general public, special populations and the elderly. Strength and
conditioning it is in fact one of the main ways to improve health
and human performance for everyone.
The challenge for everyone is to determine the appropriate
type of training not only in terms of exercises and drills used,
but most of all, to identify and understand the biological consequences of various training stimuli. Understanding how to
apply the correct modality of exercise, the correct volume and
intensity and the correct timing of various interventions is it in
fact the “holy grail” of strength and conditioning. The only way
to define it is therefore to understand more and more about the
biological principles that govern human adaptations to such
stimuli, as well as ways to measure and monitor specific adaptations to be able to prescribe the most effective and safe way of
exercising. Modern advancements in molecular biology are
now helping us understand with much greater insight how
muscle adapts to various training and nutritional regimes.
Technology solutions help us in measuring many aspects of
human performance as it happens. We now have more advanced
capabilities for prescribing “evidence-based” strength and conditioning programmes to everyone, from the general population
to the elite athlete. Our aim with this book is to collect all the
most relevant and up to date information on this topic as written
by World leaders in this field and provide a comprehensive
resource for everyone interested in understanding more about
this fascinating field.
We have structured the book to provide a continuum of
information to facilitate its use in educational settings as well
as a key reference for strength and conditioning professionals
and the interested lay public. In Section 1 we present the
biological aspects of strength and conditioning. How muscles,
bones and tendons work, how neural impulses allow muscle
activity, how genetics and bioenergetics affect muscle function
and how the cardiorespiratory system works. In section 2 we
present the latest information on how various systems respond
fpref.indd xv
and adapt to various strength and conditioning paradigms to
provide a better understanding of the implications of strength
and conditioning programmes on human physiology. Section
3 provides a detailed description of various modalities to
measure and monitor the effectiveness of strength and conditioning programmes as well as identifying ways for improving strength and conditioning programme prescriptions. Section
4 provides the latest information on practical applications and
nutritional considerations to maximise the effectiveness of
strength and conditioning programmes. Finally section 5 provides the latest guidelines to use strength and conditioning
in various populations with the safest and most effective
progressions.
The way the material has been presented varies among the
chapters. We wanted our contributors to present their area of
expertise for a varied audience ranging from sports scientists to
coaches to postgraduate students. Authors from many countries
have contributed to this book and whatever the style has been,
we are confident the material can catch the attention of every
reader.
ACKNOWLEDGEMENTS
The editors would like to thank Nicola Mc Girr, Izzy Canning,
Fiona Woods, Gill Whitley the wonderful people in the John
Wiley & Sons, Ltd. for the continuous support, guidance and
help to make this book happen.
Marco Cardinale would like to thank the numerous colleagues contributing to this book as well as the coaches, athletes
and sports scientists which over the years contributed to the
development of strength and conditioning. Thank you, my dear
wife Daniela and son Matteo for your love and support over the
years and for putting up with my odd schedules and moods over
the preparation of this project.
Robert Newton acknowledges the fantastic collaborators
that he has had the honour to work with over the past three
decades and the dedicated and hardworking students and postdocs that he has been privileged to mentor. Thank you, my dear
wife Lisa and daughter Talani for all your support and patience
through my obsession with research and teaching.
Ken Nosaka appreciates the opportunity to make this book
with many authors, Marco, Rob, and the wonderful people in
the John Wiley & Sons, Ltd. I have experienced how challenging it is to edit a book and to make an ideal book, but it was a
good lesson. Because of many commitments, I have a limited
time with my wife Kaoru and daughter Cocolo. I am so sorry,
but your support and understanding are really appreciated, and
would like to tell you that you make my life valuable.
10/18/2010 5:12:12 PM
fpref.indd xvi
10/18/2010 5:12:12 PM
List of Contributors
Per Aagaard
Institute of Sports Science and Clinical Biomechanics,
University of Southern Denmark, Odense, Denmark
Prue Cormie
School of Exercise, Biomedical and Health Sciences,
Edith Cowan University, Joondalup, WA, Australia
Chris R. Abbiss
School of Exercise, Biomedical and Health
Sciences, Edith Cowan University, Joondalup,
WA, Australia
Blair Crewther
Imperial College, Institute of Biomedical Engineering,
London UK
Tim Ackland
School of Sport Science, Exercise and Health,
University of Western Australia, WA, Australia
Jesper L. Andersen
Institute of Sports Medicine Copenhagen,
Bispebjerg Hospital, Copenhagen, Denmark
David Bishop
Institute of Sport, Exercise and Active Living (ISEAL),
School of Sport and Exercise Science,Victoria
University, Melbourne, Australia
Anthony Blazevich
School of Exercise, Biomedical and Health Sciences,
Edith Cowan University, Joondalup, WA, Australia
Marco Cardinale
British Olympic Medical Institute, Institute of Sport
Exercise and Health, University College London,
London, UK; School of Medical Sciences, University of
Aberdeen, Aberdeen, Scotland, UK
Christian Cook
United Kingdom Sport Council, London, UK
Matthew Cook
English Institute of Sport, Manchester, UK
Stuart J. Cormack
Essendon Football Club, Melbourne, Australia
flast.indd xvii
Paul Davies
English Institute of Sport, Bisham Abbey Performance
Centre, Marlow, Bucks, UK
Vincenzo Denaro
Department of Orthopaedic and Trauma Surgery,
Campus Bio-Medico University, Rome, Italy
Kevin De Pauw
Department of Human Physiology and Sports
Medicine, Faculteit LK, Vrije Universiteit Brussel,
Brussels, Belgium
Fred J. DiMenna
School of Sport and Health Sciences, University of
Exeter, Exeter, UK
Avery D. Faigenbaum
Department of Health and Exercise Science, The
College of New Jersey, Ewing, NJ, USA
Marco Gazzoni
LISiN, Dipartimento di Elettronica, Politecnico di
Torino, Torino, Italy
Olivier Girard
ASPETAR – Qatar Orthopaedic and Sports Medicine
Hospital, Doha, Qatar
Umile Giuseppe Longo
Department of Orthopaedic and Trauma Surgery,
Campus Bio-Medico University, Rome, Italy
10/18/2010 5:12:12 PM
xviii
LIST OF CONTRIBUTORS
Albert Gollhofer
Institute of Sport and Sport Science, University of
Freiburg, Germany
Thomas Muehlbauer
Institute of Exercise and Health Sciences,
University of Basel, Switzerland
Urs Granacher
Institute of Sport Science, Friedrich Schiller University,
Jena, Germany
Marco V. Narici
Institute for Biomedical Research into Human
Movement and Health (IRM), Manchester
Metropolitan University, Manchester, UK
Stuart Gray
School of Medical Sciences, College of Life
Sciences and Medicine, University of Aberdeen,
Aberdeen, UK
Markus Gruber
Department of Training and Movement Sciences,
University of Potsdam, Germany
Mark Jarvis
English Institute of Sport, Birmingham, UK
Andrew M. Jones
School of Sport and Health Sciences, University of
Exeter, Exeter, UK
Arimantas Lionikas
School of Medical Sciences, College of Life Sciences
and Medicine, University of Aberdeen,
Aberdeen, UK
Nicola A. Maffiuletti
Neuromuscular Research Laboratory, Schulthess
Clinic, Zurich, Switzerland
Robert U. Newton
School of Exercise, Biomedical and Health
Sciences, Edith Cowan University, Joondalup,
WA, Australia
Kazunori Nosaka
School of Exercise, Biomedical and Health
Sciences, Edith Cowan University, Joondalup,
WA, Australia
Jeremiah J. Peiffer
Murdoch University, School of Chiropractic and
Sports Science, Murdoch, WA, Australia
Alberto Rainoldi
Motor Science Research Center, University School
of Motor and Sport Sciences, Università degli Studi,
di Torino, Torino, Italy
Aivaras Ratkevicius
School of Medical Sciences, College of Life Sciences
and Medicine, University of Aberdeen, Aberdeen, UK
Nicola Maffulli
Centre for Sports and Exercise Medicine, Queen
Mary University of London, Barts and The London
School of Medicine and Dentistry, Mile End Hospital,
London, UK
Jörn Rittweger
Institute for Biomedical Research into Human
Movement and Health, Manchester Metropolitan
University, Manchester, UK; Institute of Aerospace
Medicine, German Aerospace Center (DLR),
Cologne, Germany
Constantinos N. Maganaris
Institute for Biomedical Research into Human
Movement and Health (IRM), Manchester
Metropolitan University, Manchester, UK
William A. Sands
Monfort Family Human Performance Research
Laboratory, Mesa State College – Kinesiology,
Grand Junction, CO, USA
Ron J. Maughan
School of Sport, Exercise and Health Sciences,
Loughborough University, Loughborough, UK
Andreas Schlumberger
EDEN Reha, Rehabilitation Clinic, Donaustauf,
Germany
Michael R. McGuigan
New Zealand Academy of Sport North Island,
Auckland, New Zealand; Auckland University of
Technology, New Zealand
Christopher S. Shaw
School of Sport and Exercise Sciences, The University
of Birmingham, UK
Romain Meeusen
Department of Human Physiology and Sports
Medicine, Faculteit LK, Vrije Universiteit Brussel,
Brussels, Belgium
flast.indd xviii
Jeremy Sheppard
Queensland Academy of Sport, Australia; School of
Exercise, Biomedical and Health Sciences, Edith
Cowan University, Joondalup,
WA, Australia
10/18/2010 5:12:12 PM
CONTRIBUTORS
xix
Matt Spencer
Physiology Unit, Sport Science Department, ASPIRE,
Academy for Sports Excellence, Doha, Qatar
Wolfgang Taube
Unit of Sports Science, University of Fribourg,
Switzerland
Filippo Spiezia
Department of Orthopaedic and Trauma Surgery,
Campus Bio-Medico University, Rome, Italy
Kevin D. Tipton
School of Sports Sciences, University of Stirling,
Stirling, Scotland, UK
Arthur Stewart
Centre for Obesity Research and Epidemiology,
Robert Gordon University, Aberdeen, UK
Valmor Tricoli
Department of Sport, School of Physical Education
and Sport, University of São Paulo, São Paulo, Brazil
Margaret E. Stone
Center of Excellence for Sport Science and Coach
Education, East Tennessee State University, Johnson
City, TN, USA
Henning Wackerhage
School of Medical Sciences, College of Life Sciences
and Medicine, University of Aberdeen, Aberdeen, UK
Michael H. Stone
Center of Excellence for Sport Science and Coach
Education, East Tennessee State University, Johnson
City, TN, USA; Department of Physical Education,
Sport and Leisure Studies,University of Edinburgh,
Edinburgh, UK; Edith Cowan University, Perth,
Australia
flast.indd xix
Warren Young
School of Human Movement and Sport Sciences,
University of Ballarat, Ballarat, Victoria. Australia
10/18/2010 5:12:12 PM
flast.indd xx
10/18/2010 5:12:12 PM
Section 1
Strength and Conditioning Biology
c01.indd 1
10/18/2010 5:11:13 PM
c01.indd 2
10/18/2010 5:11:13 PM
1.1
Skeletal Muscle Physiology
Valmor Tricoli, University of São Paulo, Department of Sport, School of Physical Education and Sport,
São Paulo, Brazil
1.1.1
INTRODUCTION
The skeletal muscle is the human body’s most abundant tissue.
There are over 660 muscles in the body corresponding to
approximately 40–45% of its total mass (Brooks, Fahey and
Baldwin, 2005; McArdle, Katch and Katch, 2007). It is estimated that 75% of skeletal muscle mass is water, 20% is
protein, and the remaining 5% is substances such as salts,
enzymes, minerals, carbohydrates, fats, amino acids, and highenergy phosphates. Myosin, actin, troponin and tropomyosin
are the most important proteins.
Skeletal muscles play a vital role in locomotion, heat production, support of soft tissues, and overall metabolism. They
have a remarkable ability to adapt to a variety of environmental
stimuli, including regular physical training (e.g. endurance or
strength exercise) (Aagaard and Andersen, 1998; Andersen
et al., 2005; Holm et al., 2008; Parcell et al., 2005), substrate
availability (Bohé et al., 2003; Kraemer et al., 2009; Phillips,
2009; Tipton et al., 2009), and unloading conditions (Alkner
and Tesch, 2004; Berg, Larsson and Tesch, 1997; Caiozzo
et al., 2009; Lemoine et al., 2009; Trappe et al., 2009).
This chapter will describe skeletal muscle’s basic structure
and function, contraction mechanism, fibre types and hypertrophy. Its integration with the neural system will be the focus of
the next chapter.
1.1.2 SKELETAL MUSCLE
MACROSTRUCTURE
Skeletal muscles are essentially composed of specialized contracting cells organized in a hierarchical fashion supported by
a connective tissue framework. The entire muscle is surrounded
by a layer of connective tissue called fascia. Underneath the
fascia is a thinner layer of connective tissue called epimysium
which encloses the whole muscle. Right below is the perimysium, which wraps a bundle of muscle fibres called fascicle (or
fasciculus), thus; a muscle is formed by several fasciculi.
Lastly, each muscle fibre is covered by a thin sheath of collagenous connective tissue called endomysium (Figure 1.1.1).
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
c01.indd 3
Directly beneath the endomysium lies the sarcolemma, an
elastic membrane which contains a plasma membrane and a
basement membrane (also called basal lamina). Sometimes, the
term sarcolemma is used as a synonym for muscle-cell plasma
membrane. Among other functions, the sarcolemma is responsible for conducting the action potential that leads to muscle
contraction. Between the plasma membrane and basement
membrane the satellite cells are located (Figure 1.1.2). Their
regenerative function and possible role in muscle hypertrophy
will be discussed later in this chapter.
All these layers of connective tissue maintain the skeletal
muscle hierarchical structure and they combine together to form
the tendons at each end of the muscle. The tendons attach
muscles to the bones and transmit the force they generate to the
skeletal system, ultimately producing movement.
1.1.3 SKELETAL MUSCLE
MICROSTRUCTURE
Muscle fibres, also called muscle cells or myofibres, are long,
cylindrical cells 1–100 μm in diameter and up to 30–40 cm in
length. They are made primarily of smaller units called myofibrils which lie in parallel inside the muscle cells (Figure 1.1.3).
Myofibrils are contractile structures made of myofilaments
named actin and myosin. These two proteins are responsible for
muscle contraction and are found organized within sarcomeres
(Figure 1.1.3). During skeletal muscle hypertrophy, myofibrils
increase in number, enlarging cell size.
A unique characteristic of muscle fibres is that they are
multinucleated (i.e. have several nuclei). Unlike most body
cells, which are mononucleated, a muscle fibre may have 250–
300 myonuclei per millimetre (Brooks, Fahey and Baldwin,
2005; McArdle, Katch and Katch 2007). This is the result of
the fusion of several individual mononucleated myoblasts
(muscle’s progenitor cells) during the human body’s development. Together they form a myotube, which later differentiates
into a myofibre. The plasma membrane of a muscle cell is often
called sarcolemma and the sarcoplasm is equivalent to its cytoplasm. Some sarcoplasmic organelles such as the sarcoplasmic
reticulum and the transverse tubules are specific to muscle cells.
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
10/21/2010 3:16:19 PM
4
SECTION 1
Fascia
STRENGTH AND CONDITIONING BIOLOGY
Tendon
Endomysium
Basal lamina
Muscle
Plasma membrane
Myonucleus
Epimysium
Muscle Fiber
Satellite cell
Endomysium
Basal lamina
Plasma membrane
(sarcolemma)
Myonucleus
Muscle fiber
Muscle Fiber
Perimysium
Figure 1.1.2 Illustration of a single multinucleated muscle fibre and
satellite cell between the plasma membrane and the basal lamina
Connective tissue
Figure 1.1.1 Skeletal muscle basic hierarchical structure. Adapted
from Challis (2000)
1.1.3.1
Sarcomere and myofilaments
A sarcomere is the smallest functional unit of a myofibre and
is described as a structure limited by two Z disks or Z lines
(Figure 1.1.3). Each sarcomere contains two types of myofilament: one thick filament called myosin and one thin filament
called actin. The striated appearance of the skeletal muscle is
the result of the positioning of myosin and actin filaments inside
each sarcomere. A lighter area named the I band is alternated
with a darker A band. The absence of filament overlap confers
a lighter appearance to the I band, which contains only actin
filaments, while overlap of myosin and actin gives a darker
appearance to the A band. The Z line divides the I band in two
equal halves; thus a sarcomere consists of one A band and two
half-I bands, one at each side of the sarcomere. The middle of
the A band contains the H zone, which is divided in two by the
M line. As with the I band, there is no overlap between thick
and thin filaments in the H zone. The M line comprises a
number of structural proteins which are responsible for anchoring each myosin filament in the correct position at the centre of
the sarcomere.
On average, a sarcomere that is between 2.0 and 2.25 μm
long shows optimal overlap between myosin and actin filaments, providing ideal conditions for force production. At
lengths shorter or larger than this optimum, force production is
compromised (Figure 1.1.4).
c01.indd 4
The actin filament is formed by two intertwined strands (i.e.
F-actin) of polymerized globular actin monomers (G-actin).
This filament extends inward from each Z line toward the centre
of the sarcomere. Attached to the actin filament are two regulatory proteins named troponin (Tn) and tropomyosin (Tm) which
control the interaction between actin and myosin. Troponin is a
protein complex positioned at regular intervals (every seven
actin monomers) along the thin filament and plays a vital role in
calcium ion (Ca++) reception. This regulatory protein complex
includes three components: troponin C (TnC), which binds
Ca++, troponin T (TnT), which binds tropomyosin, and troponin
I (TnI), which is the inhibitory subunit. These subunits are in
charge of moving tropomyosin away from the myosin binding
site on the actin filament during the contraction process.
Tropomyosin is distributed along the length of the actin filament in the groove formed by two F-actin strands and its main
function is to inhibit the coupling between actin and myosin
filaments from blocking active actin binding sites (Figure 1.1.5).
The thick filament is made mostly of myosin protein. A
myosin molecule is composed of two heavy chains (MHCs) and
two pairs of light chains (MLCs). It is the MHCs that determines muscle fibre phenotype. In mammalian muscles, the
MHC component exists in four different isoforms (types I, IIA,
IIB, and IIX), whereas the MLCs can be separated into two
essential LCs and two regulatory LCs. Myosin heavy and light
chains combine to fine tune the interaction between actin and
myosin filaments during muscle contraction. A MHC is made
of two distinct parts: a head (heavy meromyosin) and a tail
(light meromyosin), in a form that may be compared to that of
a golf club (Figure 1.1.6).
Approximately 300 myosin molecules are arranged tail-totail to constitute each thick filament (Brooks, Fahey and
Baldwin, 2005). The myosin heads protrude from the filament;
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CHAPTER 1.1
Muscle fibre
Dark
A band
SKELETAL MUSCLE PHYSIOLOGY
5
Light
I band
Myofibril
Section
of a myofibril
A band I band
Z disc
Actin: Thin filament
Myosin: Thick filament
Sarcomere
Cross-bridges
M line
A band
I band
Z disc
Tension (percent of maximum)
Figure 1.1.3 Representation of a muscle fibre and myofibril showing the structure of a sarcomere with actin and myosin filaments. Adapted
from Challis (2000)
100
80
60
40
20
0
Optimal Length
1.2 μm
2.1 μm 2.2 μm
3.6 μm
Sarcomere Length
Figure 1.1.4 Skeletal muscle sarcomere length–tension relationship
c01.indd 5
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6
SECTION 1
STRENGTH AND CONDITIONING BIOLOGY
Myosin heavy chain
G actin
actin-binding site
Troponin I
Myosin head
mATPase
Troponin C
Myosin tail
F actin
Troponin T
Tropomyosin
Ca++
Tn T
Myosin Filament
Tn C
Tn I
Actin
Myosin
active binding site
Figure 1.1.5 Schematic drawing of part of an actin filament
showing the interaction with tropomyosin and troponin complex
Figure 1.1.6 Schematic organization of a myosin filament, myosin
heavy chain structure, and hexagonal lattice arrangement between
myosin and actin filaments
Vinculin
α-integrin
β-integrin
Actin filament
Myosin
filament
Z disk
M line
C-protein
Desmin
Titin
α-actinin
Z disk
Nebulin
Figure 1.1.7 Illustration of the structural proteins in the sarcomere
each is arranged in a 60 ° rotation in relation to the preceding
one, giving the myosin filament the appearance of a bottle
brush. Each myosin head attaches directly to the actin filament
and contains ATPase activity (see Section 1.1.5). Actin and
myosin filaments are organized in a hexagonal lattice, which
means that each myosin filament is surrounded by six actin filaments, providing a perfect match for interaction during contraction (Figure 1.1.6).
A large number of other proteins can be found in the
interior of a muscle fibre and in sarcomeres; these constitute
the so-called cytoskeleton. The cytoskeleton is an intracellular
system composed of intermediate filaments; its main functions
c01.indd 6
are to (1) provide structural integrity to the myofibre, (2) allow
lateral force transmissions among adjacent sarcomeres, and
(3) connect myofibrils to the cell’s plasma membrane. The
following proteins are involved in fulfilling these functions
(Bloch and Gonzalez-Serratos, 2003; Hatze, 2002; Huijing,
1999; Monti et al., 1999): vinculin, α- and β-integrin (responsible for the lateral force transmission within the fibre), dystrophin (links actin filaments with the dystroglycan and
sarcoglycan complexes, which are associated with the sarcolemma and provide an extracellular connection to the basal
lamina and the endomysium), α-actinin (attaches actin
filaments to the Z disk), C protein (maintains the myosin
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CHAPTER 1.1
SKELETAL MUSCLE PHYSIOLOGY
7
Plasma membrane (sarcolemma)
Action potential
Lateral sacs
Myofibrils
Ca++
Transverse tubule
Ca++
Sarcoplasmic reticulum
Triad
Figure 1.1.8 Representation of the transverse tubules (T tubules) and sarcoplasmic reticulum system
tails in a correct spatial arrangement), nebulin (works as a
ruler, assisting the correct assembly of the actin filament),
titin (contributes to secure the thick filaments to the Z lines),
and desmin (links adjacent Z disks together). Some of these
proteins are depicted in Figure 1.1.7.
1.1.3.2 Sarcoplasmic reticulum and
transverse tubules
The sarcoplasmic reticulum (SR) of a myofibre is a specialized
form of the endoplasmic reticulum found in most human body
cells. Its main functions are (1) intracellular storage and (2)
release and uptake of Ca++ associated with the regulation of
muscle contraction. In fact, the release of Ca++ upon electrical
stimulation of the muscle cell plays a major role in excitation–
contraction coupling (E-C coupling; see Section 1.1.4). The SR
can be divided into two parts: (1) the longitudinal SR and (2)
the junctional SR (Rossi and Dirksen, 2006; Rossi et al., 2008).
The longitudinal SR, which is responsible for Ca++ storage and
uptake, comprises numerous interconnected tubules, forming an
intricate network of channels throughout the sarcoplasm and
around the myofibrils. At specific cell regions, the ends of the
longitudinal tubules fuse into single dilated sacs called terminal
cisternae or lateral sacs. The junctional SR is found at the junction between the A and the I bands and represents the region
responsible for Ca++ release (Figure 1.1.8).
The transverse tubules (T tubules) are organelles that carry
the action potential (electrical stimulation) from the sarcolemma surface to the interior of the muscle fibre. Indeed, they
are a continuation of the sarcolemma and run perpendicular to
the fibre orientation axis, closely interacting with the SR. The
association of a T tubule with two SR lateral sacs forms a
structure called a triad which is located near each Z line of a
sarcomere (Figure 1.1.8). This arrangement ensures synchronization between the depolarization of the sarcolemma and the
release of Ca++ in the intracellular medium. It is the passage of
an action potential down the T tubules that causes the release
of intracellular Ca++ from the lateral sacs of the SR, causing
muscle contraction; this is the mechanism referred to as E-C
coupling (Rossi et al., 2008).
c01.indd 7
1.1.4
CONTRACTION MECHANISM
1.1.4.1 Excitation–contraction
(E-C) coupling
A muscle fibre has the ability to transform chemical energy into
mechanical work through the cyclic interaction between actin
and myosin filaments during contraction. The process starts
with the arrival of an action potential and the release of Ca++
from the SR during the E-C coupling. An action potential is
delivered to the muscle cell membrane by a motor neuron
through the release of a neurotransmitter named acetylcholine
(ACh). The release of ACh opens specific ion channels in the
muscle plasma membrane, allowing sodium ions to diffuse
from the extracellular medium into the cell, leading to the
depolarization of the membrane. The depolarization wave
spreads along the membrane and is carried to the cell’s interior
by the T tubules. As the action potential travels down a T
tubule, calcium channels in the lateral sacs of the SR are opened,
releasing Ca++ in the intracellular fluid. Calcium ions bind to
troponin and, in the presence of ATP, start the process of skeletal muscle contraction (Figure 1.1.9).
1.1.4.2 Skeletal muscle contraction
Based on a three-state model for actin activation (McKillop and
Geeves, 1993), the thin filament state is influenced by both Ca++
binding to troponin C (TnC) and myosin binding to actin. The
position of tropomyosin (Tm) on actin generates a blocked, a
closed, or an open state of actin filament activation. When
intracellular Ca++ concentration is low, and thus Ca++ binding
to TnC is low, the thin filament stays in a blocked state because
Tm position does not allow actin–myosin interaction. However,
the release of Ca++ by the SR and its binding to TnC changes
the conformational shape of the troponin complex, shifting the
actin filament from a blocked to a closed state. This transition
allows a weak interaction of myosin heads with the actin filament, but during the closed state the weak interaction between
myosin and actin does not produce force. Nevertheless, the
weak interaction induces further movements in Tm, shifting the
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8
SECTION 1
STRENGTH AND CONDITIONING BIOLOGY
Axon
Vesicles
Mithocondria
Release site
Acetylcholine
Action potential
Sarcoplasmic reticulum
Myofibrils
T tubule
Ca++ release
Troponin complex
Actin filament
Myosin filament
Tropomyosin
active binding
site
Figure 1.1.9 Excitation–contraction coupling and the sequence of events that will lead to skeletal muscle contraction
Myosin Filament
Myosin head
Open state (attached)
Actin Filament
Actin binding site
ATP
Detached
ADP + Pi
ATP hydrolysis
Release of Pi
Power stroke
Open state (attached)
Figure 1.1.10 Cyclic process of muscle contraction
c01.indd 8
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CHAPTER 1.1
1.1.5
MUSCLE FIBRE TYPES
The skeletal muscle is composed of a heterogeneous mixture of
different fibre types which have distinct molecular, metabolic,
structural, and contractile characteristics, contributing to a
range of functional properties. Skeletal muscle fibres also have
an extraordinary ability to adapt and alter their phenotypic
profile in response to a variety of environmental stimuli.
Muscle fibres defined as slow, type I, slow red or slow
oxidative have been described as containing slow isoform contractile proteins, high volumes of mitochondria, high levels of
myoglobin, high capillary density, and high oxidative enzyme
capacity. Type IIA, fast red, fast IIA or fast oxidative fibres
have been characterized as fast-contracting fibres with high
oxidative capacity and moderate resistance to fatigue. Muscle
fibres defined as type IIB, fast white, fast IIB (or IIx), or fast
c01.indd 9
9
ATPase activity (mmol l–1s–1)
Figure 1.1.11 Photomicrograph showing three different muscle fibre
types
0.5
Shortening velocity (a.u.)
actin filament from the closed to the open state, resulting in a
strong binding of myosin heads. In the open state, a high affinity
between the myosin heads and the actin filament provides an
opportunity to force production.
The formation of the acto-myosin complex permits the
myosin head to hydrolyse a molecule of ATP and the free
energy liberated is used to produce mechanical work (muscle
contraction) during the cross-bridge power stroke (Vandenboom,
2004). Cross-bridges are projections from the myosin filament
in the region of overlap with the actin filament. The release of
ATP hydrolysis byproducts (Pi and ADP) induces structural
changes in the acto-myosin complex that promote the crossbridge cycle of attachment, force generation, and detachment.
The force-generation phase is usually called the ‘power stroke’.
During this phase, actin and myosin filaments slide past each
other and the thin filaments move toward the centre of the
sarcomere, causing its shortening (Figure 1.1.10). Each crossbridge power stroke produces a unitary force of 3–4 pico
Newtons (1 pN = 10−12 N) over a working distance of 5–15
nanometres (1 nm = 10−9 m) against the actin filament (Finer,
Simmons and Spudich, 1994). The resulting force and displacement per cross-bridge seem extremely small, but because billions of cross-bridges work at the same time, force output and
muscle shortening can be large.
Interestingly, the myosin head retains high affinity for only
one ligand (ATP or actin) at a time. Therefore, when an ATP
molecule binds to the myosin head it reduces myosin affinity
for actin and causes it to detach. After detachment, the myosin
head rapidly hydrolyses the ATP and uses the free energy to
reverse the structural changes that occurred during the power
stroke, and then the system is ready to repeat the whole cycle
(Figure 1.1.10). If ATP fails to rebind (or ADP release is inhibited), a ‘rigour ’ cross-bridge is created, which eliminates the
possibility of further force production. Thus, the ATP hydrolysis cycle is associated with the attachment and detachment of
the myosin head from the actin filament (Gulick and Rayment,
1997). If the concentration of Ca++ returns to low levels, the
muscle is relaxed by a reversal process that shifts the thin filament back toward the blocked state.
SKELETAL MUSCLE PHYSIOLOGY
0.4
0.3
0.2
0.1
0
I
IIA
IIA-B
IIB
Figure 1.1.12 Representation of the relationship between skeletal
muscle fibre type, mATPase activity, and muscle shortening velocity
glycolytic present low mitochondrial density, high glycolytic
enzyme activity, high myofibrilar ATPase (mATPase) activity,
and low resistance to fatigue (Figure 1.1.11).
Several methods, including mATPase histochemistry,
immunohistochemistry, and electrophoretic analysis of myosin
heavy chain (MHC) isoforms, have been used to identify myofibre types. The histochemical method is based on the differences
in the pH sensitivity of mATPase activity (Brooke and Kaiser,
1970). Alkaline or acid assays are used to identify low or high
mATPase activity. An ATPase is an enzyme that catalyses the
hydrolysis (breakdown) of an ATP molecule. There is a strong
correlation between mATPase activity and MHC isoform
(Adams et al., 1993; Fry, Allemeier and Staron, 1994; Staron,
1991; Staron et al., 2000) because the ATPase is located at the
heavy chain of the myosin molecule. This method has been used
in combination with physiological measurements of contractile
speed; in general the slowest fibres are classified as type I
(lowest ATPase activity) and the fastest as type IIB (highest
ATPase activity), with type IIA fibres expressing intermediate
values (Figure 1.1.12). The explanation for these results is that
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10
SECTION 1
STRENGTH AND CONDITIONING BIOLOGY
the velocity of the interaction between myosin and actin depends
on the speed with which the myosin heads are able to hydrolyse
ATP molecules (see Section 1.1.4).
Immunohistochemistry explores the reaction of a specific
antibody against a target protein isoform. In this method,
muscle fibre types are determined on the basis of their immunoreactivity to antibodies specific to MHC isoforms. An electrophoretic analysis is a fibre typing method in which an
electrical field is applied to a gel matrix which separates MHC
isoforms according to their molecular weight and size (MHCIIb
is the largest and MHCI is the smallest). Because of the difference in size, MHC isoforms migrate at different rates through
the gel. Immunohistochemical and gel electrophoresis staining
procedures are applied in order to visualize and quantify MHC
isoforms.
Independent of the method applied, the results have revealed
the existence of ‘pure’ and ‘hybrid’ muscle fibre types (Pette,
2001). A pure fibre type contains only one MHC isoform,
whereas a hybrid fibre expresses two or more MHC isoforms.
Thus, in mammalian skeletal muscles, four pure fibre types can
be found: (1) slow type I (MHCIβ), (2) fast type IIA (MHCIIa),
(3) fast type IID (MHCIId), and (4) fast type IIB (MHCIIb)
(sometimes called fast type IIX fibres) (Pette and Staron, 2000).
Actually, type IIb MHC isoform is more frequently found in
rodent muscles, while in humans type IIx is more common
(Smerdu et al., 1994).
Combinations of these major MHC isoforms occur in hybrid
fibres, which are classified according to their predominant
isoform. Therefore, the following hybrid fibre types can be
distinguished: type I/IIA, also termed IC (MHCIβ > MHCIIa);
type IIA/I, also termed IIC (MHCIIa > MHCIβ); type IIAD
(MHCIIa > MHCIId); type IIDA (MHCIId > MHCIIa); type
IIDB (MHCIId > MHCIIb); and type IIBD (MHCIIb > MHCIId)
(Pette, 2001). All these different combinations of MHCs contribute to generating the continuum of muscle fibre types represented below (Pette and Staron, 2000):
TypeI ↔ TypeIC ↔ TypeIIC ↔ TypeIIA ↔ TypeIIAD ↔
TypeIIDA ↔ TypeIID ↔ TypeeIIDB ↔ TypeIIBD ↔ TypeIIB
Despite the fact that chronic physical exercise, involving
either endurance or strength training, appears to induce transitions in the muscle fibre type continuum, MHC isoform changes
are limited to the fast fibre subtypes, shifting from type IIB/D
to type IIA fibres (Gillies et al., 2006; Holm et al., 2008;
Putman et al., 2004).The reverse transition, from type IIA to
type IIB/D, occurs after a period of detraining (Andersen and
Aagaard, 2000; Andersen et al., 2005). However, it is still
controversial whether training within physiological parameters
can induce transitions between slow and fast myosin isoforms
(Aagaard and Thorstensson, 2003). The amount of hybrid fibre
increases in transforming muscles because the coexistence of
different MHC isoforms in a myofibre leads it to adapt its phenotype in order to meet specific functional demands.
How is muscle fibre type defined? It appears that even in
foetal muscle different types of myoblast exist and thus it is
likely that myofibres have already begun their differentiation
into different types by this stage (Kjaer et al., 2003);
c01.indd 10
innervation, mechanical loading or unloading, hormone profile,
and ageing all play a major role in phenotype alteration.
The importance of innervation in the determination of specific myofibre types was demonstrated in a classic experiment
of cross-reinnervation (for review see Pette and Vrbova, 1999):
fast muscle phenotype became slow once reinnervated by a
slow nerve, while a slow muscle became fast when reinnervated
by a fast nerve. Nevertheless, motor nerves are not initially
required for the differentiation of fast and slow muscle fibres,
although innervation is later essential for muscle growth and
survival. Motor innervation is also involved in fibre type differentiation during foetal development.
Curiously, unloaded muscles show a tendency to convert
slow fibres to fast ones (Gallagher et al., 2005; Trappe et al.,
2004, 2009). This shift in fibre type profile was observed in
studies involving microgravity conditions (spaceflight or bedrest models). It appears that slow MHC isoforms are more
sensitive to the lack of physical activity than fast isoforms
(Caiozzo et al., 1996, 2009; Edgerton et al., 1995).
A hormonal effect on muscle fibre phenotypes is markedly
observed with thyroid hormones. In skeletal muscles, thyroid
hormones reduce MHCI gene transcription, while they stimulate transcription of MHCIIx and MHCIIb. The effects on the
transcription of the MHCIIa gene are muscle-specific: transcription is activated in slow muscles such as soleus and
repressed in fast muscles such as diaphragm (Baldwin and
Haddad, 2001; DeNardi et al., 1993). Thus, in general, reduced
levels of thyroid hormone cause fast-to-slow shifts in MHC
isoform expression, whereas high levels of thyroid hormone
cause slow-to-fast shifts (Canepari et al., 1998; Li et al., 1996;
Vadászová et al., 2004).
In addition to muscle atrophy and a decrease in strength,
ageing may cause fast-to-slow fibre type transitions (Canepari
et al., 2009; Korhonen et al., 2006). Degenerative processes in
the central nervous system (CNS) and/or peripheral nervous
system (PNS), causing denervation (selective loss of fast αmotor neurons) and reinnervation (with slow α-motor neurons),
physical inactivity, and altered thyroid hormone levels, may
contribute to the observed atrophy and potential loss of fast
muscle fibres in elderly people.
1.1.6
MUSCLE ARCHITECTURE
Skeletal muscle architecture is defined as the arrangement of
myofibres within a muscle relative to its axis of force generation
(Lieber and Fridén, 2000). Skeletal muscles present a variety
of fasciculi arrangements but they can be described mostly as
fusiforms or pennate muscles. A fusiform muscle has fibres
organized in parallel to its force-generating axis and is described
as having a parallel or longitudinal architecture. A pennate
muscle has fibres arranged at an oblique angle to its forcegenerating axis (Figure 1.1.13).
Muscle fibre arrangement has a functional significance and
the effect of muscle design on force production and contraction
velocity is remarkable. In a fusiform muscle, the myofibres
cause force production to occur directly at the tendon; the parallel arrangement allows fast muscle shortening. In a pennate
10/18/2010 5:11:14 PM
CHAPTER 1.1
SKELETAL MUSCLE PHYSIOLOGY
11
Figure 1.1.13 Muscle architecture: three different arrangements of
muscle fibres (fusiform, unipennate, and bipennate). The angle at
resting length in mammalian muscles varies from 0 ° to 30 °
muscle, fascicule angle affects force transmission and decreases
shortening velocity. Because fibres are orientated at an angle
relative to the axis of force generation, not all fibre tensile force
is transmitted to the tendons and only a component of fibre force
production is actually transmitted along the muscle axis, in
proportion to the pennation angle cosine (Figure 1.1.14). It
seems that pennate arrangement is detrimental to muscle
strength performance as it results in a loss of force compared
with a muscle of the same mass and fibre length but zero pennation angle. However, a muscle with pennate fibres is able to
generate great amounts of force. In fact, high-intensity strength
training causes increases in pennation angle (Aagaard et al.,
2001; Kawakami, Abe and Fukunaga, 1993; Kawakami et al.,
1995; Reeves et al., 2009; Seynnes, de Boer and Narici, 2007)
which enhance the muscle’s ability to pack more sarcomeres
and myofibres, creating a large physiological cross-sectional
area (PCSA). A PCSA is measured perpendicular to the fibre
orientation, whereas an anatomical cross-sectional area (ACSA)
is measured perpendicular to the muscle orientation. A large
PCSA positively affects the force-generating capacity of the
muscle, compensating for the loss in force transmission due to
increases in pennation angle (Lieber and Fridén, 2000).
Two other important parameters in architectural analysis are
muscle length and fibre length. Muscle velocity is proportional
to muscle/fibre length. Muscles with similar PCSAs and pennation angles but different fibre lengths have different velocity
outputs. The muscle with the longest fibres presents greater
contraction velocity, while shorter muscles are more suitable
for force production with low velocity. Thus, antigravity short
extensor muscles are designed more for force production, while
longer flexors are for long excursions with higher velocity. The
soleus muscle, with its high PCSA and short fibre length, suitable for generating high force with small excursion, is a good
example of an antigravity postural muscle, while the biceps
femoris is an example of a long flexor muscle suitable for generating high velocity with long excursion.
c01.indd 11
Figure 1.1.14 Representation of the effect of muscle fibre
arrangement. Fibres orientated parallel to the axis of force generation
transmit all of their force to the tendon. Fibres orientated at a 30 °
angle relative to the force-generation axis transmit part of their force
to the tendon, proportional to the angle cosine. Adapted from Lieber
(1992)
1.1.7
HYPERTROPHY AND
HYPERPLASIA
A good example of skeletal muscle’s ability to adapt to environmental stimuli is the hypertrophy that occurs after a period
of strength training. Hypertrophy can be defined as the increase
in muscle fibre size and/or muscle mass due to an accumulation
of contractile and noncontractile proteins inside the cell (Figure
1.1.15). Increased rate of protein synthesis, decreased rate of
protein breakdown, or a combination of both of these factors,
is responsible for muscle hypertrophy (Rennie et al., 2004).
Most of us are in a state of equilibrium between muscle protein
synthesis and protein degradation; thus muscle mass remains
constant. Muscle size and muscle mass can also be enlarged by
way of hyperplasia, which is an increase in the number of
myofibres. However, the suggestion that new muscle fibres may
form in human adults as a result of strength training is still
highly controversial (Kadi, 2000). Hyperplasia has been demonstrated following strength training in some animal models
(Antonio and Gonyea, 1993; 1994; Tamaki et al., 1997) but the
evidence in human subjects is unclear (Kelley, 1996; McCall
et al., 1996).
Hypertrophy-orientated strength training affects all muscle
fibre types, however type II fast fibres have usually shown a
more pronounced response than type I slow fibres (Aagaard
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12
SECTION 1
STRENGTH AND CONDITIONING BIOLOGY
Strength Training stimuli
IGF-1/MGF
P13K
Akt
Figure 1.1.15 Magnetic resonance image of the quadriceps femoris
before and after a period of strength training
mTOR
4EBP-1
p70S6k
eIF4E
↑Protein synthesis
et al., 2001; Cribb and Hayes, 2006; Verdijk et al., 2009). It
appears that type II fibres possess a greater adaptive capacity
for hypertrophy than type I fibres. This is interesting because it
has been demonstrated that muscle protein synthesis does not
differ between fibre types after a bout of strength training exercise (Mittendorfer et al., 2005). Similarly, satellite cells, which
are important contributors to muscle hypertrophy (see Section
1.1.8), are equally distributed in human vastus lateralis type I
and type II fibres (Kadi, Charifi and Henriksson, 2006).
The question of how mechanical signals provided by
strength training are translated into increased muscle protein
synthesis and hypertrophy has not been fully answered. It is
beyond the scope of this chapter to deeply explain the possible mechanism and intracellular pathways involved in muscle
hypertrophy (for more details see Spangenburg, 2009; Zanchi
and Lancha, 2008). In brief, high tension applied over skeletal
muscles during strength training stimulates the release of
growth factors such as insulin-like growth factor 1 (IGF-1).
It has been shown that this hormone is involved in muscle
hypertrophy through autocrine and/or paracrine mechanisms
(Barton-Davis, Shoturma and Sweeney, 1999). IGF-1 is a
potent activator of the protein kinase B (Akt)/mammalian target
of rapamycin (mTOR) signalling pathway, which is a key
regulator in protein synthesis. Activation of Akt is mediated
by the IGF-1/phosphatidylinositol-3 kinase (PI3K) pathway.
Once activated, Akt activates mTOR, which in turn activates
70 kDa ribosomal S6 protein kinase (p70S6k), a positive regulator of protein translation (Baar and Esser, 1999). The degree
of activation of p70S6k is closely associated with the subsequent protein synthesis and muscle growth. mTOR also inhibits
the activity of 4E binding protein 1 (4E-BP1), a negative
regulator of the protein-initiation factor eIF-4E, which is
c01.indd 12
Hypertrophy
Figure 1.1.16 Schematic illustration of the effect of strength
training stimuli on activation of the hypertrophy pathway
involved in translation initiation and like p70S6k contributes
to enhanced protein synthesis (Koopman et al., 2006). Any
alteration in mTOR activation will result in changes in p70s6k
activation and 4EBP-1 inactivation, ultimately affecting the
initiation of protein synthesis and causing increases in muscle
size and mass (Figure 1.1.16). It appears that muscle tension
per se may also stimulate skeletal muscle growth through a
mechanism called mechano-transduction; the regulation of the
Akt/mTOR signalling pathway in response to mechanical
stimuli is still not well understood however (Rennie et al.,
2004).
1.1.8
SATELLITE CELLS
Adult skeletal muscle contains a cell population with stem celllike properties called satellite cells (SCs) (Hawke, 2005). These
are located at the periphery of myofibres, between the basal
lamina and the sarcolemma (Figure 1.1.2) (Vierck et al., 2000;
Zammit, 2008). Skeletal muscle SCs are undifferentiated quiescent myogenic precursors that display self- renewal properties (Huard, Cao and Qu-Petersen, 2003), which means that they
can generate daughter cells which can become new SCs (Kadi
10/18/2010 5:11:14 PM
CHAPTER 1.1
et al., 2004; Zammit and Beauchamp, 2001). They serve as
reserve cells and are recruited when myofibre growth and/or
regeneration after injury is needed. In response to signals associated with muscle damage, mechanical loading, and exercise,
SCs leave the quiescent state, become activated, and reenter the
cell cycle (Hawke and Garry, 2001; Tidball, 2005). After activation, these cells proliferate and migrate to the site of injury
to repair or replace damaged myofibres by fusing together to
create a myotube or by fusing to existing myofibres (Hawke,
2005; Machida and Booth, 2004).
It appears that the fusion of SCs to existing myofibres is also
critical for increases in fibre cross-sectional area. This physiological event takes into consideration the concept of the myonuclear domain or DNA unit, which suggests that each
myonucleus manages the production of mRNA and protein
synthesis for a specific volume of sarcoplasm (Adams, 2002;
Kadi and Thornell, 2000; Petrella et al., 2008). It has been
proposed that there may be a limit on the amount of expansion
a myonuclear domain can undergo during hypertrophy (i.e. a
domain ceiling size) (Kadi et al., 2004). A limit indicates that
an expansion of the myonuclear domain toward a threshold
>2000 μm2/nucleus (Petrella et al., 2006), or between 17 and
25% of the fibre’s initial size (Kadi et al., 2004), may put each
myonucleus under greater strain, thus increasing the demand
for new myonuclei to make continued growth possible (Petrella
et al., 2008).
This implies that increases in muscle fibre size (i.e. hypertrophy) must be associated with a proportional increase in
myonucleus number. However, muscle fibres are permanently
differentiated, and therefore incapable of producing additional
myonuclei through mitosis (Hawke and Garry, 2001; Machida
and Booth, 2004). Nevertheless, it has been shown that myonucleus number increases during skeletal muscle hypertrophy,
in order to maintain the cytoplasm-to-myonucleus ratio (Allen
et al., 1995; Petrella et al., 2006), and the only alternative
source of additional myonuclei is the pool of SCs (Kadi,
2000; Rosenblatt and Parry, 1992). In adult skeletal muscles,
it has been observed that satellite cell-derived myonuclei are
incorporated into muscle fibres during hypertrophy (Kadi and
Thornell, 2000). Following the initial increase in muscle fibre
size that occurs via increased mRNA activity and protein
c01.indd 13
SKELETAL MUSCLE PHYSIOLOGY
13
accretion, the incorporation of additional myonuclei in muscle
fibres represents an important mechanism for sustaining muscle
fibre enlargement (Petrella et al., 2006). Incorporated satellite
cell-derived myonuclei are no longer capable of dividing,
but they can produce muscle-specific proteins that increase
myofibre size (Allen, Roy and Edgerton, 1999), resulting in
hypertrophy.
The mechanisms by which skeletal muscle SCs are activated
and incorporated into growing myofibres are still unclear but it
has been suggested that they are modulated by cytokines and
autocrine/paracrine growth factors (Hawke and Garry, 2001;
Petrella et al., 2008). For example, strength exercises induce
damage to the sarcolemma, connective tissue, and muscle fibre
structural and contractile proteins, initiating an immune
response which then attracts macrophages to the damaged area.
Macrophages secrete a number of cytokines, which regulate the
SCs pool. In order to regenerate the damaged myofibres, SCs
differentiate and fuse together to generate a myotube, which
then fuses to the damaged muscle fibre, repairing the injury.
Despite the differences between skeletal muscle regeneration and hypertrophy, both processes share similarities regarding SCs activation, proliferation, and differentiation. It is
believed that muscle-loading conditions (i.e. strength training)
stimulate the release of growth factors (IGF-1 and MGF),
which affects SC activation, proliferation and differentiation
(Adams and Haddad, 1996; Bamman et al., 2007; Vierck
et al., 2000). Insulin-like growth factor-1 (IGF-1) and its
isoform mechano-growth factor (MGF) are potent endocrine
and skeletal muscle autocrine/paracrine growth factors. IGF-1
is upregulated in response to hypertrophic signals in skeletal
muscle and promotes activation, proliferation and fusion of
the SCs. During skeletal muscle hypertrophy, SCs fuse to the
existing myofibres, essentially donating their nuclei, whereas
in regeneration from more extensive muscle damage SCs fuse
together to generate a new myotube, which repairs damaged
fibres (Hawke, 2005).
The ageing process decreases the number of SCs and negatively affects their proliferative capacity; these two factors may
be related to the atrophy and poor muscle regeneration described
in some elderly individuals (Crameri et al., 2004; Kadi et al.,
2004).
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14
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1.2
Neuromuscular Physiology
Alberto Rainoldi1 and Marco Gazzoni2, 1 University School of Motor and Sport Sciences, Università degli Studi di
Torino, Motor Science Research Center, Torino, Italy, 2 LISiN, Politecnico di Torino, Dipartimento di Elettronica,
Torino, Italy
1.2.1
THE NEUROMUSCULAR SYSTEM
Movement involves the interaction between the nervous system
and the muscles. The nervous system generates the signals
which tell the muscles to activate and the muscles provide the
proper force.
1.2.1.1
Motor units
The skeletal muscles consist of up to a million muscle fibres.
To coordinate the contraction of all these fibres, they are subdivided into functional units: the motor units. A motor unit
consists of one motoneuron (located in the spinal cord and
brainstem) and the fibres which it innervates (Figure 1.2.1).
The fibres belonging to a single motor unit are localized
within a region of the muscle cross-section (up to 15%) and are
intermingled with fibres belonging to other motor units.
Moreover, some evidence exists for the muscle organization
in neuromuscular compartments; that is, regions of muscle supplied by a primary branch of the muscle nerve. A single muscle
can consist of several distinct regions, each with a different
physiological function (English, 1984; Fleckenstein et al.,
1992).
Motor unit types
Many criteria and terminologies have been used to classify the
types of fibre or motor unit (see Chapter 1.1). Histochemical,
biochemical, and molecular properties are used to measure the
mechanisms responsible for physiological properties (e.g. contraction speed, magnitude of force, fatigue resistance). Direct
physiological measurements of contraction speed, magnitude of
force, and fatigue resistance have also been used to distinguish
motor unit types.
Although the measurement of motor unit properties in
human muscle results in a less discrete classification scheme
than that for muscle fibres, motor unit activity is often discussed
in terms of the following scheme. The smaller slow-twitch
motor units have been called ‘tonic units’. Histochemically,
they are the smaller units (type I), and metabolically they have
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
c02.indd 17
fibres rich in mitochondria, are highly capillarized, and therefore have a high capacity for aerobic metabolism. Mechanically,
they produce twitches with a low peak tension and a long time
to peak (60–120 ms). The larger fast-twitch motor units are
called ‘phasic units’ (type II). They have less mitochondria, are
poorly capillarized, and therefore rely on anaerobic metabolism. The twitches have larger peak tensions in a shorter time
(10–50 ms).
Although commonly adopted, the motor unit scheme
described above does not appear to be appropriate for human
muscles on the basis of the following considerations: (1) investigators have been unable to clearly distinguish motor unit types
in human muscle (Fuglevand, Macefield and Bigland-Ritchie,
1999); (2) the first motor units activated in a voluntary contraction can be either slow-twitch or fast-twitch (Van Cutsem et al.,
1997); and (3) the cross-sectional area of human muscle fibres
often does not increase from type I to type Il (Harridge et al.,
1996; Miller et al., 1993).
1.2.1.2
Muscle receptors
A number of different peripheral receptors are located within
muscle, tendon, and fascia. Their role is to provide afferent
information from the periphery to the CNS following the typical
loop of any omeostatic system. They in fact continuously
provide feedback to allow the CNS to properly maintain human
body ‘stability’.
In general, afferent axons are classified with respect to their
cross-section in four groups, from the larger, with faster conduction velocity (group I), to the smaller, with slower conduction velocity (group IV).
Muscle spindles
Spindles are fusiform organs which lie in parallel with skeletal
muscle fibres. There are more than 25 000 spindles throughout
the human body; their role is to provide feedback information
to changes in muscle length (Proske, 1997). Each spindle is
innervated by gamma motonenurons; such neural input comes
from the spinal cord. Group I afferents end in a spiral shape on
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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Cell body
Nucleus
In the spinal
cord
1.2.1.3 Nervous and muscular
conduction velocity
Axon
Synapase
In the
muscle
Muscle fibre
Figure 1.2.1 A motor unit consists of its motor nerve, which
branches out to form connections to many muscle fibres through
synapses, called motor end plates
the muscle spindle; when the fibre is stretched, the spiral is
modified and an action potential is transmitted to the CNS. In
the same way, when the whole muscle is passively stretched,
the spindle spirals ‘feel’ the deformation and forward the information to the CNS.
Tendon organs
These are placed within the tendon and, due to their position,
are often described as ‘organs in series with skeletal muscle
fibres’, whereas muscle spindles are in parallel with them, as
described above. These organs are activated as a consequence
of (active or passive) stretching of the muscle, thus of the connective tissue attachments, and of the group I afferents which
are branched in the myotendinous junction. For these reasons,
these organs are considered as muscle force sensors; their
threshold of excitation depends on the mode of activation
(active or passive).
Joint receptors
Unlike muscle spindles and tendon organs, joint receptors vary
in relation to their location and function. They are usually
served by neurons with group II, III, and IV afferents. For
c02.indd 18
instance, Ruffini-ending mechanoreceptors are able to monitor
joint position and displacement, angular velocity, and intraarticular pressure (Johannsson, Sjölander and Sojka, 1991).
Pacinian corpuscles seem to be able to detect acceleration of
the joint (Bell, Bolanowsky and Holmes, 1994). Golgi endings
are corpuscles with a behaviour similar to that of tendon organs.
They play a protective role monitoring tension in ligaments,
especially at the extremes of the range of motion. In general,
joint receptors seem to act on a single joint indirectly, modulating the activity of the muscle spindle and thus influencing the
α-motor neuron output.
Conduction velocity is the velocity at which action potentials
propagate along the fibre. Conduction velocities of both axonal
and sarcolemmal action potentials vary with the diameter of the
axon. The larger the diameter, the greater the conduction
velocity.
Nervous and muscular propagations are sustained by two
different mechanisms: the saltatory conduction in myelinated
fibres from one node of Ranvier to the next, and the depolarization front induced by sodium and potassium currents, respectively. As a consequence, two different average conduction
velocities are available, the former in the range 90–105 m/s and
the latter in the range 3–5 m/s. These two ranges correspond to
two extremely different tasks: (1) to provide information to the
CNS at a velocity fast enough to ensure proper feedback (within
safe reaction time and throughout the body); (2) to allow fast
contraction of muscle fibres, which can have a maximum emilength of 15 cm (as in the case of the longest muscle, the sartorius muscle, for instance). Since muscle fibres can change their
cross-section area (hypertrophy) and, in some conditions, their
number (hyperplasia), the conduction velocity and thus the
MVC can be increased even if the fibre type remains unchanged.
1.2.1.4 Mechanical output production
The force that a muscle exerts during a contraction depends on
the excitation provided by the nervous system (the number of
motor neurons that are activated and the rates at which they
discharge), the mechanical properties of the muscle, and the
muscle architecture.
As described in Chapter 1.1, for a given level of excitation,
the muscle force depends on muscle length (force–length relation) and on the rate of change in length (force–velocity
relation).
The basic contractile properties of muscle, as characterized
by the force–length and force–velocity relations of the single
fibre, are influenced by the way in which the fibres are organized to form a muscle (Lieber and Friden, 2000; Russell,
Motlagh and Ashley, 2000). Muscle fibres can be in series, in
parallel, or at an angle to the line of pull of the muscle (angle
of pennation). In-series arrangement maximizes the maximum
10/18/2010 5:11:15 PM
CHAPTER 1.2
NEUROMUSCULAR PHYSIOLOGY
19
shortening velocity and the range of motion of the muscle,
whereas in-parallel arrangement maximizes the force the
muscle can exert. In pennated muscles, the contribution of the
fibres to the muscle force varies with the cosine of the angle of
pennation.
thick filaments to the thin filaments. As the length of the muscle
changes, the number of actin binding sites available for the
cross-bridges changes, and this influence the force a muscle can
exert. The relationship between maximum tetanic force and
sarcomere length is illustrated in Figure 1.2.4.
Motor units and muscle twitch
Force–velocity relation
The contractile property of a motor unit is described by the
force–time response (twitch) to a single excitatory input (Figure
1.2.2a). All motor units have the same characteristic twitch
shape, described by: (1) the time for the tension to reach the
maximum (contraction time), (2) the magnitude of the peak
force, and (3) the time the force takes to decline to one-half of
its peak value (half-relaxation time).
Hill (1938) characterized the force–velocity relationship and
emphasized the importance of this parameter in the study of
muscle function.
The force–velocity curve relation is reported in Figure 1.2.5.
It shows a decrease of force with an increase in the speed at
which the muscle shortens and an increase of force with an
increase of muscle-lengthening velocity. Isometric contractions
are along the zero-velocity axis of this graph and can be considered as a special case within the range of possible velocities.
It should be noted that this curve represents the characteristics
at a certain muscle length.
It is important to underline that the force–length and force–
velocity relations describe the force exerted by a muscle at a
given length or at a given constant rate of change in length.
During movement these conditions are rarely satisfied and the
force exerted by muscle often deviates from that expected on
the basis of the described relations.
Force–frequency relation
Motor units are rarely activated to produce individual twitches.
They usually receive as input several action potentials, resulting
in overlapping twitch responses, producing a force 1.5–10.0
times greater than the twitch force. The degree to which the
twitches summate depends on the rate at which the action potentials are discharged, producing the force–frequency relation
(Figure 1.2.3b). With an increase in the frequency of the action
potentials, the force profile (tetanus) changes from an irregular
profile (unfused) (Figure 1.2.2c) to a smooth plateau (fused
tetanus) (Figure 1.2.2d). The capability of the motor unit to
exert force is assessed from the peak force of a single fused
tetanus, not from the single twitch.
a
Force–length relation
The cross-bridge theory of muscle contraction suggests that
muscle force is generated by cross-bridges extending from the
a
b
Peak Force
CT HRT
b
c
d
Figure 1.2.2 Twitch and tetanic responses of motor units in a cat
hindlimb muscle. (a) Motor unit twitch (contraction time
(CT) = 24 ms; half relaxation time (HRT) = 21 ms; peak
force = 0.03 N). (b) Twitch responses for fast- and slow-twitch motor
units. (c) Unfused tetanus. (d) Fused tetanus
c02.indd 19
Figure 1.2.3 Force–frequency relation for motor units in human toe
extensor muscles. (a) Motor units activated by intraneural stimulation
(upper trace) evoke a force in the dorsiflexor muscles (lower trace).
(b) Force was normalized to the maximum value for each motor unit
to produce the force–frequency relation for 13 motor units. The
increase in force when action potential rate goes from 5 to 10 Hz is
not the same as that due to increasing the rate from 20 to 25 Hz, even
though there is a difference of 5 Hz in each case. The greatest
increase in force (steepest slope) occurs at intermediate discharge
rates (9–12 Hz). Reproduced from Macefield, Fuglevand & BiglandRitchie. J Neurophysiol. 1996 Jun;75(6):2509–19.
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20
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STRENGTH AND CONDITIONING BIOLOGY
Muscle Tension
Max.
Tension M.U.4
Threshold
M.U.4
Threshold
M.U.3
Max. Tension M.U.3
Max. Tension M.U.2
Threshold
M.U.2
Max. Tension M.U.1
T
M.U.1
Figure 1.2.4 Variation of maximum tetanic force with sarcomer
length. Insets show degree of filament overlap of four different
sarcomer lengths. At resting length, about 2.5 μm, there is a
maximum number of cross-bridges between the filaments, and
therefore a maximum tension is possible. As the muscle lengthens,
the filaments are pulled apart, the number of cross-bridges reduces,
and tension decreases. At full length, about 4.0 μm, there are no
cross-bridges and the tension reduces to zero. As the muscle shortens
to less than resting length, there is an overlapping of the cross-bridges
that results in a reduction of tension, which continues until a full
overlap occurs, at about 1.5 μm. From Edman and Reggiani (1987)
Force
100%
75%
M.U.2
M.U.3
M.U.4
Figure 1.2.6 Example of a force curve resulting from the
recruitment of motor units. The smallest motor unit (MU 1) is
recruited first, usually at an initial frequency ranging from about 5 to
13 Hz. Tension increases as MU 1 fires more rapidly, until a certain
tension is reached, at which MU 2 is recruited. Here MU 2 starts
firing at its initial low rate and further tension is achieved by the
increased firing of both MU 1 and 2. At a certain tension MU 1 will
reach its maximum firing rate (15–60 Hz) and will therefore be
generating its maximum tension
1.2.1.5 Muscle force modulation
Each muscle has a finite number of motor units, each of which
is controlled by a separate nerve ending. Excitation of each unit
is an all-or-nothing event.
As previously stated, the force that a muscle can exert is
varied through: (1) the number of motor units that are active
(motor unit recruitment), (2) the stimulation rate of motor units
(discharge rate modulation).
ax
M
um
im
50%
ion
ns
Te
25%
Motor unit recruitment
–
Lengthen
0
Shorten
+
Velocity
Figure 1.2.5 Force–velocity characteristics of skeletal muscle,
showing a decrease of tension as muscle shortens and an increase as
it lengthens. All such characteristics must be taken as the muscle
shortens or lengthens at a given length, and the length must be
reported. A family of curves results if different levels of muscle
activation are plotted. Figure shows curves at 25, 50, 75, and 100%
levels of activation
c02.indd 20
In 1938, Denny-Brown and Pennybacker reported that a movement always appears to be accomplished by the activation of
motor units in a relatively fixed sequence (orderly recruitment).
To increase the force exerted by a muscle, additional motor
units are activated (recruited); once a motor unit is recruited, it
remains active until the force declines. To reduce the exerted
force, motor units are sequentially inactivated (derecruited) in
reverse order; that is, the last motor unit recruited is the first
derecruited (Figure 1.2.6). The recruitment of motor units
follows the size principle (Henneman et al., 1974), which states
that the order in which the motor neurons are activated is
10/18/2010 5:11:15 PM
NEUROMUSCULAR PHYSIOLOGY
Each dot is a
discharge of a MU.
Isometric
contraction,
biceps brachii
21
10.0
force
7.5
time
5.0
force (% MVC)
20
19
18
17
16
15
14
13
12
11
10
9
8
7
6
5
4
3
2
1
dicharge rate
MU number
CHAPTER 1.2
2.5
0
1
2
3
4
5
6
7
time (s)
8
9
10
11
12
Figure 1.2.7 Recruitment and discharge pattern during an abductor digiti minimi muscle contraction in which force increases to 10% of
maximum. Each dot represents the instantaneous discharge frequency of a motor unit (inverse of the interspike interval) and each horizontal line
represents the discharge rate of a motor unit over time. The order of motor unit recruitment and derecruitment can be seen, associated with the
produced muscle force
dictated by the motor neuron size, proceeding from smallest to
largest. Figure 1.2.7 depicts an example of a force curve resulting from the recruitment of motor units. The process of increasing tension, reaching new thresholds, and recruiting another,
larger motor unit continues until maximum voluntary contraction is reached. Force is reduced by the reverse process: successive reduction of firing rates and dropping out of the larger
units first.
Discharge rate
When a motor unit is recruited and the force exerted by the
muscle continues to increase, the rate at which the motor neuron
discharges usually increases (Figure 1.2.8).
The minimum rate at which motor neurons discharge action
potentials repetitively during voluntary contractions is about
5–7 Hz. Maximum discharge rates vary across muscles (35–
40 Hz for first dorsal interosseus, 25–35 Hz for adductor digiti
minimi and adductor pollicis, 20–25 Hz for biceps brachii and
extensor digitorum communis, 11 Hz for soleus).
The contribution of motor unit recruitment to muscle force
varies between muscles. In some muscles, all motor units
are recruited when the force reaches about 50% of maximum,
in other muscles recruitment continues up to 85% of the
maximum force (De Luca et al., 1982; Kukulka and Clamann,
1981; Van Cutsem et al., 1997). The increase in muscle force
beyond the upper limit of motor unit recruitment is accomplished entirely through variation in the discharge rate of
action potentials.
c02.indd 21
Figure 1.2.8 Modulation of discharge rate by four motor units
during a gradual increase and then decrease in the force (thick line)
exerted by the knee extensor muscles. Each thin line represents the
activity of a single motor unit, with recruitment occurring at the
leftmost dot on each thin line. MU 1, for example, was recruited at a
force of about 18% of maximum with an initial discharge rate of
9 Hz, which increased to 15 Hz at the peak force (Person and Kudina,
1972)
10/18/2010 5:11:16 PM
22
SECTION 1
STRENGTH AND CONDITIONING BIOLOGY
Experimental examples of abnormal
motor unit recruitment
Although the orderly recruitment of motor units has been verified in many studies, it can vary under some conditions.
At the motor unit level, changes in recruitment order have
been observed as a consequence of manipulation of sensory
feedback (Garnett and Stephens, 1981; Kanda, Burke and
Walmsley, 1977) and during performance of lengthening contractions (Nardone, Romanò and Schieppati, 1989). One way to
demonstrate this effect is to determine the recruitment order of
pairs of motor units in the absence and presence of a perceptible
cutaneous sensation elicited by electrical stimulation of the
skin. In the absence of this stimulus, one motor unit is recruited
at a lower force than the other. In the presence of the cutaneous
sensation, however, the unit with the higher recruitment threshold is activated first. This reversal of recruitment order is useful
if the cutaneous sensation requires a rapid response.
At the whole-muscle level one example of an alteration in
recruitment order is the paw-shake response. This behaviour is
elicited in animals when a piece of tape sticks to a paw; the
animal’s response is to vigorously shake the paw in an attempt
to remove the tape. In normal activities, such as standing,
walking, and running, the force exerted by soleus (slow-twitch
muscle) remains relatively constant across tasks, while that
exerted by medial gastrocnemius (fast-twitch muscle) increases
with the power demand of the task. In the paw-shake response
fast-twitch muscles are mainly activated. The recruitment
change in a group of synergist muscles allows the animal to
move its limb rapidly.
Westad, Westgaard and De Luca (2003) observed abnormal
motor unit recruitment in human trapezius; low-threshold motor
units recruited at the start of the contraction were observed to
stop firing while motor units of higher recruitment threshold
stayed active. Casale et al. (2009) observed that recruitment
during voluntary contractions was altered in fibromyalgic
patients. Experimental findings suggest that fibromyalgic
patients use compensatory motor strategies to compensate
chronic fatigue, recruiting motor units in a different manner
than that predicted by Henneman’s principle.
Discharge patterns
In addition to motor unit recruitment and discharge rate, the
force exerted by a muscle is influenced by the discharge pattern
of motor units. The discharge patterns known as ‘common
drive’ and ‘motor unit synchronization’ refer to the temporal
relation of the action potentials firing among different motor
units. Common drive describes the correlated variation in the
average discharge rate of concurrently active motor. Motor unit
synchronization quantifies the amount of correlation between
the timing of the individual action potentials discharged by
active motor units.
1.2.1.6
Electrically elicited contractions
Muscle contraction can be inducted by selective electrical stimulation (NMES) of a nerve branch or of a motor point of a
c02.indd 22
muscle; this allows ‘disconnection’ of the investigated portion
of muscle from the CNS and control of motor unit activation
frequency. By changing the intensity of the electrical stimulation, it is possible to change the number of activated motor
units. The effectiveness of NMES was proved to be greater in
unhealthy subjects (for instance, during and post immobilization) than in normal people, for whom voluntary exercise was
found more favourable (Bax, States and Verhagen, 2005;
Delitto and Snyder-Mackler, 1990).
In contrast to the order in which motor units are activated
during voluntary contractions, the classic view is that largediameter axons are more easily excited by imposed electric
fields, which would reverse the activation order of motor units
in electrically evoked contractions compared with voluntary
contractions. However, some studies demonstrate that neuromuscular electrical stimulation tends to activate motor units
in a similar order to that which occurs during voluntary contractions, with more variability with respect to voluntary
contractions.
Recent works (Collins, 2007) demonstrate that the electrically elicited contractions do not only act on the peripheral
system (that is, behind the motor junction), but that the simultaneous depolarization of sensory axons can also contribute
to the contractions by the synaptic recruitment of spinal
motoneurons.
1.2.2
MUSCLE FATIGUE
Fatigue is a daily experience corresponding to lack of maintenance of a physical activity. This is actually the definition of
‘mechanical fatigue’, which refers intuitively to output (force,
torque, motor task) reduction. This visible impairment is
induced by a physiological process, which can imply different
sites and contributions to the fatigue; they can be schematically
listed as follows:
Central fatigue (of the primary motor cortex and of central
drive to motor neurons).
Fatigue of the neuromuscular junction (in the activation of
muscle and motor units and in neuromuscular propagation).
Peripheral fatigue (of the excitation–contraction coupling, of
the availability of metabolic substrates, of muscle blood
flow).
1.2.2.1 Central and peripheral fatigue
The mechanical output production, as described above, can
decrease during exertion for a number of reasons. Twenty years
ago a technique was devised to highlight the amount of central
drive reduction (Hales and Gandevia, 1988); the issue of spinal
and supraspinal factors in human muscle fatigue was clearly
described in a recent extended review (Gandevia, 2001). The
technique consisted in the so-called ‘twitch interpolation’:
supramaximal electric shocks are applied to the nerve during
10/18/2010 5:11:16 PM
CHAPTER 1.2
23
Power
CV normalized rate of change (%/s)
an MVC task. If such an electrical stimulation increases the
force output, the central drive during the contraction is not
maximal and the subject is showing central fatigue. In such a
way it is also possible to directly assess the ability of a subject
to provide true MVC. Moreover, it is possible to monitor the
time course of other physical variables such as force or torque,
power, angular velocity of a joint, motor unit firing rate, and
motor unit synchronization.
Prolonged activity can also impair neuromuscular propagation, decreasing force output due to a failure of axonal action
potential, a failure of the excitation–secretion coupling, a depletion of the neurotransmitter, or a decrease of the sensitivity of
postsynaptic receptors (Spira, Yarom and Parnas, 1976).
Peripheral fatigue is defined as the changes occurring within
the muscle, behind the neuromuscular junction. Thus it is possible to study the electromyographic fatigue; that is, all the
changes occurring in the EMG signal during a sustained voluntary contraction or an electrically elicited contraction (M
wave). Starting from such signals, it is possible to monitor the
variation in time of the conduction velocity of muscle fibre
action potentials (or of the M wave), which represents the most
physiological parameter actually available from the EMG
signal (Farina et al., 2004). Innovative techniques (see below)
allow tracking of single motor units, enabling us to obtain the
conduction velocity distribution of the pool of active and
recordable motor units and to visualize bidimensional maps of
electrical activity over the skin.
Further fatigue within the muscle is also related to variation
in metabolic substrates. This means a number of changes that
can occur in active muscle fibres: depletion of glycogen
(Hermansen, Hultman and Saltin, 1967), increase of H+ and Pi
concentrations (Vøllestad, 1995), reduction of intracellular pH
(Brody et al., 1991), and reduction of oxygen supply due to the
increase of intramuscular pressure (Sjøgaard, Savard and Juel,
1988).
NEUROMUSCULAR PHYSIOLOGY
Endurance
1.0
0.5
7%
230%
0.0
Intermittent
Continuous
Figure 1.2.9 Normalized (with respect to initial values) rates of
change of CV in continuous and intermittent contractions for both
groups of athletes. The increment of fatigue in the continuous with
respect to the intermittent contraction was greater in the endurance
than in the power athletes. Mean ± SD absolute values are reported
by 200% when endurance athletes were asked to move from
intermittent (characterized by 1 s of rest in between) to continuous contraction (of the same workload), whereas powertrained athletes did not modify their fatigue rate (Rainoldi
et al., 2008). That approach is now proposed as a noninvasive
technique to distinguish between two extremely different
phenotypes.
1.2.3
MUSCLE FUNCTION
ASSESSMENT
1.2.2.2 The role of oxygen availability
in fatigue development
1.2.3.1 Imaging techniques
As described above, the amount of oxygen supply is one of
the pivotal factor affecting contraction and causing fatigue.
Casale et al. (2004) concluded that acute exposure to hypobaric
hypoxia did not significantly affect muscle fibre membrane
properties (no peripheral effect) but that it did impact on motor
unit control properties (central control strategies for adaptation). Hence the lack of oxygen induced by high altitude was
able to induce central effects aimed to recruiting more fast
motor units than the equivalent effects at sea level, allowing
maintenance of the requested force task. Thus it is possible
to assess whether variation in EMG manifestations of fatigue
are induced by a central or a peripheral adaptation by means
of two different contraction modalities (voluntary or electrically induced).
A specific protocol was recently designed to highlight the
effect of oxygen availability in endurance- and power-trained
athletes. As depicted in Figure 1.2.9, fatigue index increased
The advent of modern imaging techniques offers new approaches
for monitoring musculoskeletal function and structure. The
most widely used techniques are T1- and T2-weighted magnetic
resonance (MR) imaging, cine phase-contrast MR imaging, MR
elastography, and ultrasonography (Segal, 2007).
T1- and T2-weighted MR imaging is useful for determining
muscle cross-sectional area noninvasively and in vivo, allowing
monitoring adaptations in muscle cross-sectional area consequent to disease, immobilization, rehabilitation, or exercise.
Muscle MR imaging has been used to analyse which muscles
or regions of muscles are active during functional tasks, but
low-level muscle activity is detected by EMG before it can be
detected by MR imaging (Cheng et al., 1995).
T2 time mapping showed the capability, under some circumstances, to evaluate the spatial localization of activity within
portions of muscles, allowing the study of neuromuscular compartments (Akima et al., 2000; Segal and Song, 2005).
c02.indd 23
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24
SECTION 1
STRENGTH AND CONDITIONING BIOLOGY
One potentially important use for MR imaging is the monitoring of the adaptation of muscle activation in response to
fatigue, CNS injuries, diseases, or therapies (Akima et al., 2002;
Pearson, Fouad and Misiaszek, 1999).
Cine phase-contrast MR imaging has been proposed to visualize the differential displacement of muscle fibres within a
muscle during movement (Pappas et al., 2002; Pelc et al., 1994)
and to provide muscle architectural information (Finni et al.,
2003) (Figures 1.2.10 and 1.2.11).
MR elastography is a method that allows the estimation of
the mechanical properties of tissues during both passive and
active movements (Basford et al., 2002; Heers et al., 2003). A
high correlation between MR elastography wavelengths and
electromyographic activity has been found (Heers et al., 2003),
suggesting that MR elastography is a valid approach for the
noninvasive assessment of muscle properties in the context of
muscle activity.
Ultrasonography has been used to examine musculotendinous structure and movement (Fukashiro et al., 1995;
Kawakami, Ichinose and Fukunaga, 1998). This approach does
not require a special room, as MR imaging does; it requires only
an ultrasonography transducer, sophisticated analysis software,
and, most importantly, skilful application. The technique is
completely noninvasive, is carried out in vivo, and is essentially
real-time.
1.2.3.2 Surface EMG as a muscle
imaging tool
Surface EMG (sEMG) has been considered the gold standard
for the noninvasive measurement of muscle activity in human
subjects and provides a standard method for monitoring temporal information about muscle activity. In the last 10 years,
research activity has been moved toward sEMG recording with
two-dimensional array systems, the so-called high-density
sEMG. This technique, by using multiple closely spaced electrodes overlying an area of the skin, provides not only temporal
information, but also spatial distribution of the electrical activity over the muscle. It thus opens new possibilities for studying
muscle characteristics, transforming the amount and quality of
information actually available. High-density sEMG allows the
Figure 1.2.10 Examples of the cine phase contrast images obtained using the velocity-encoded MRI pulse sequence. The optical density of
each pixel is proportional to the velocity of the volume of tissue represented by the pixel. Each image is the same sagittal section of the leg of a
normal subject during an isometric plantarflexion action. The left side of the image is anterior and the right side is posterior. The velocities and
direction of the movement of a given point are reflected in the optical densities, with the lower scale of optical densities representing movement
in one direction and the upper scale of optical densities representing movements in the opposite direction. Note the difference in velocities within
and between the muscles of the anterior and posterior compartments (Lai, Sinha, Hodgson and Edgerrton, unpublished observations)
Figure 1.2.11 Examples of the cine phase contrast images using the velocity-encoded MRI pulse sequence at different sagittal planes of the leg
of a normal subject during an isometric action. Left side of the image is anterior, right side is posterior (Lai, Sinha, Hodgson and Edgerrton,
unpublished observations)
c02.indd 24
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CHAPTER 1.2
estimation of muscle anatomical characteristics such as muscle
fibre length, muscle fibre orientation, and localization of the
innervation zones (Farina and Merletti, 2004; Lapatki et al.,
2006). Moreover, it allows the estimation of motor unit location
(Drost et al., 2007; Roeleveld and Stegeman, 2002), decomposition of the sEMG interference signal into the constituent trains
NEUROMUSCULAR PHYSIOLOGY
25
of motor unit action potentials (MUAPs), and analysis of single
motor unit properties (De Luca et al., 2006; Holobar and
Zazula, 2004; Kleine et al., 2007). The information that can be
extracted from high-density sEMG signals has been shown to
be relevant for both physiological studies and clinical applications (Figures 1.2.12 and 1.2.13).
1.2.3.3 Surface EMG for noninvasive
neuromuscular assessment
Figure 1.2.12 Change of activity distribution (interpolated RMS
map) over the biceps brachii during a slow flexion of the elbow. As
the elbow flexes by 80 ° the innervation zone (IZ) moves in the
proximal direction by 2–3 cm. It is evident that the single electrode
pair at A would indicate a decrease of muscle activity while an
electrode pair placed in B would indicate an increase. This
demonstrates the need for 2D electrode arrays
A huge effort was made over the last 20 years to assess the
repeatability and affordability of the sEMG technique based on
the differential montage (with a couple or an array of electrodes). A number of clear findings are now available in different fields. For an in-depth description we refer the reader to
Merletti and Parker (2004) and to the following reviews: Drost
et al. (2006), Farina et al. (2004), Merletti, Rainoldi and Farina
(2001), Merletti, Farina and Gazzoni (2003), Mesin, Merletti
and Rainoldi (2009), Roeleveld and Stegeman (2002),
Staudenmann et al. (2010), Stegeman et al. (2000), Zwarts and
Stegeman (2003), Zwarts, Drost and Stegeman (2000) and
Zwarts et al. (2004), among others, which cover different applications and topics.
It is possible to conclude that if the maximum care were
applied in order to reduce the number of confounding factors
then any change in the EMG signal would contribute to a
wider definition of electromyographic fatigue. Hence we conclude that the time is right to accept the use of such an
approach in recording the complexity of the human system.
To study human movement means studying the neuromuscular
system from a number of different points of view. The electric
signal generated during a contraction is now ready to be
disentangled.
Figure 1.2.13 Example of the use of high-density SEMG for the determination of endplate position and muscle-fibre orientation. A sequence of
interpolated monopolar amplitude maps illustrates topographically the initiation of the potential (latencies 19 and 20) and its conduction in the
upper and lower part of the DAO muscle. Endplate position and muscle-fibre orientation were determined by localizing the grid areas of
maximal amplitude (area size was 1/2 IED in both dimensions) in the interpolated monopolar amplitude maps at the latencies of MUAP
initiation or termination. Reproduced from Lapatki et al., J Neurophysiol. 2006 Jan;95(1):342–54.
c02.indd 25
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SECTION 1
STRENGTH AND CONDITIONING BIOLOGY
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1.3
Bone Physiology
Jörn Rittweger, Institute for Biomedical Research into Human Movement and Health, Manchester Metropolitan
University, Manchester, UK and Institute of Aerospace Medicine, German Aerospace Center (DLR),
Cologne, Germany
1.3.1
INTRODUCTION
Bones are living organs. Yet they have traditionally been
regarded as a matter of anatomical study rather than being of
interest to the physiologist. Access to the cells residing in their
hard tissue is inherently difficult to obtain and recent research
suggests that their cells originate from stem cells located far
from their final location. Therefore, despite the fact that the
outlines of our bones are conserved long after death, bone
physiology remains an elusive process, and its study requires
interdisciplinary approaches, plus a good degree of ‘indirect’
thinking.
This chapter begins with an overview of bone anatomy
(=playground), going on to discuss the different bone cells
(=players), then a brief introduction to bone mechanics is given
(=scope of the game) and finally current concepts of bones
adaption are discussed (=tactics of the game).
1.3.2
BONE ANATOMY
The principle role of bones is to provide mechanical rigidity.
The skeleton provides the muscles with a framework to act
upon. Bones also protect soft tissue organs (e.g. brain, heart).
In itself, the term ‘bone’ is ambiguous, as it describes an organ
(e.g. the femur or the mandible), a tissue (e.g. compact or
trabecular bone), and a material.
1.3.2.1
Bones as organs
Bones first evolved as cartilaginous organs in fish. The conquest
of land stipulated larger musculoskeletal forces and thus the
evolution of bones as more rigid instruments. Accordingly, the
cartilaginous fish bones have been replaced by ‘proper ’ bone
tissue in land-living vertebrates. Interestingly, ontogeny reenacts the phylogenetic replacement of cartilaginous tissue, as
bones developmentally emerge from mesenchyme or cartilage
by intramembranous and endochondral ossification, respectively. Such transformations of other tissues into bone do not
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
c03.indd 29
normally take place later in life, but there are some exceptions
to this rule. In myositis ossificans, for example, bone tissue
emerges within skeletal muscle, often after trauma (Geschickter
and Maseritz, 1938). In fibrodysplasia ossificans progressiva, a
rare autosomal dominant disorder with impaired BMP-4 signalling, virtually all soft tissues are turned into bone (Kaplan
et al., 2006; Shore et al., 2006). Finally, and much more commonly, osteophytes (or bone spurs) in osteoarthritis develop
from fibrocartilage (Gilbertson, 1975). These examples may
demonstrate that the capability of ossification is retained
throughout life, but that the signals to induce this process are
normally lacking.
Most bone surfaces are covered with periosteum, an epithelium containing blood vessels and nerve fibres. Among the
nerve fibres, there are many nociceptors, which mediate pain
perception in fractures and contusions.
There are two different kinds of mechanical interface to
bones. First, joint surfaces are covered by hyaline cartilage with
low frictional coefficient, typically around 0.001 (Özkaya and
Nordin, 1998). Joints can thus transmit only compressive
forces. Second, entheses constitute contact zones with tendons,
ligaments or skeletal muscle and can be either fibrous or fibrocartilaginous. They convey tensile and shear forces. Their projections into the bone are known as Sharpey’s fibres.
All bones in land-living vertebrates have a comparatively
smooth outer surface. This layer is called the cortex (Latin for
‘bark’). Bone cortices can be wafer-thin in some places, but
examples up to 30 cm thick have been found in some extinct
sauropods. With the exception of air-filled wing bones in some
birds, the interior of all bones is filled up with marrow. This can
be either fatty or red (= haematopoietic). Marrow fat is probably
of some importance, as it is spared during starvation. However,
its precise physiological role is unknown (Currey, 2003).
Bones have different shapes. They can be long (e.g. femur),
short (e.g. calcaneus), flat bones (e.g. sternum), irregular (e.g.
vertebra) or sesamoid1 (e.g. patella). Within the long bones,
1
A sesmoid bone is one that is engulfed by a tendon and is primarily loaded in
tension. It serves to reduce shear strains where the line of action of a force is
diverted.
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
10/21/2010 3:16:22 PM
SECTION 1
STRENGTH AND CONDITIONING BIOLOGY
b
a
Distal Tibia Design
12
1000
10
800
8
600
6
c
400
4
2
200
Area
BMC
0
Bone Mineral Content
[mg/mm]
30
0
0
10
20
30
40
50
Length [%]
proximal
distal
Distal
End
Mid
Shaft
Figure 1.3.1 Principle design of long bones. (a) Replica of a ‘typical’ bone, utilized for nonscientific purposes in the street carnival of Cologne,
Germany, in 2009. Anatomically, no such bone exists. Nevertheless, this mock-up is recognized as a bone even under conditions of impaired
brain function (carnival). Therefore, it seems to be exemplary for the principle design of long bones. (b) Total bone area and bone mineral
content (BMC), as assessed in the distal tibia of 10 young healthy males by peripheral quantitative computed tomography (pQCT). As can be
seen, there is a disproportionate increase in total bone area towards the distal end of the tibia, without an increase in bone mineral content. This
is because of the trabacularization towards the end, which helps to spread the forces over a larger surface. Unpublished data by Rittweger et al.
(c) pQCT scan of a human metatarsal. Fine struts of trabecular bone branch of the cortex in order to support the joint surface. The presence of
trabeculae explains how total bone area in Figure 1.3.1b can be increased without increases in bone area
material than bone (Yamada and Evans, 1970). When physiologically loaded, the same forces pass along the axis of the long
bones and across the joints.2 In order to support the forces,
therefore, joint surfaces must be larger than bone cross-sectional
areas (see Figure 1.3.1a,b). On the other hand, bone material is
approximately twice as dense3 as the rest of our body. In order
to reduce the bone’s mass, therefore, the sub-cortical bone of
our joints is ‘spongy’ and light, rather than compact and heavy
(see Figure 1.3.1c), and the shaft is slender.
1.3.2.2 Bone tissue
Figure 1.3.2 Trabecular bone of a vertrebral body in a rat, assessed
by micro-CT. Whilst rods predominate close to the endplates (top and
bottom), mainly plates are found in the central part. Image courtesy
of Jürg Gasser
there are three different zones. The zone beyond the growth
plate (=physis) is called the epiphysis, the zone next to it the
metaphysis, and the central part of the shaft is the diaphysis.
The principle design of long bones is so typical that it is
recognized by children. To understand this design, we have to
consider the fact that joint cartilage is a substantially weaker
c03.indd 30
Bone tissue is either compact or trabecular. Trabecular bone,
also called spongy bone or cancellous bone, is made up of
interconnected rods and plates and can be found in the subcortical zones of the joints and in the interior parts of flat bones
and irregular bones. Its bone volume fraction is typically around
25%, although this varies widely and can reach values above
50% in horse’s leg bones (Figure 1.3.2).
Compact4 bone is a tissue in which the bone material is
densely packed. It can be found in the shafts of the long bones.
The tissue organization of compact bone implies a low surfaceto-volume ratio, which reduces accessibility of compact bone
2
This is because the forces that load our bones arise from muscle contractions,
and these muscles pass one or more joints.
3
The term ‘dense’ refers to Archimedes’ density (=mass per volume).
4
The terms ‘compact’ and ‘cortical’ are often used interchangeably, which
strictly speaking is not correct.
10/18/2010 5:11:17 PM
CHAPTER 1.3
tissue and may be one of the reasons for the low turnover rate
observed in the deeper layers of compact bone (Parfitt, 2002).
Both cancellous bone and compact bone tissue are made up
of stacked layers known as lamellae. In lamellar compact bone,
these lamellae are stacked in parallel upon each other (see
Figure 1.3.4) such that the ‘grain’ is rotated by a constant
amount between layers. In Haversian bone, lamellae are
arranged in a pattern of concentric rings (see Figure 1.3.3). In
woven bone this regular pattern is lost and the lamellae are
without any clear organization.5 Woven bone formation occurs
only under extreme overloading and may perhaps be understood
as some kind of ‘panic’ reaction to this.
Since bone material is solid, specific pores within the
compact bone tissue are required to permit blood and nerve
supply. They are called Volkmann canals in lamellar bone and
Haversian canals in Haversian bone.
BONE PHYSIOLOGY
A
Interstitial
lamellae
Osteocytes
Haversian
canal
Cement line
100 µm
B
5
4
1
3
x
1.3.2.3 The material level: organic and
inorganic constituents
x
Bone, as a material, consists of an organic and an inorganic
phase. Each of these contributes in a different way to the overall
material properties, and two simple experiments can inform us
about the respective role of each phase. First, demineralization6
of a bone dissolves the mineral (or inorganic) phase (= portion)
to leave the organic phase behind. This is a fluffy fabric, very
similar to a tendon, which is rigid (and strong) in tension, but
not in compression or shear loading. Conversely, burning the
organic phase7 and keeping the mineral phase in place alters a
bone’s colour slightly, but leaves its shape intact. It continues
to be considerably rigid in compression, but a gentle knock can
atomize it – the material has become brittle, similar to glass.
Assigning single properties to the bone material’s constituent
is a useful first didactic step. However, it should be realized that
a material’s overall properties ultimately arise from the interplay of all its constituents (Currey, 2002).
The organic phase constitutes approximately two thirds of
the bone material’s volume, but only one third of its dry mass.
Its main constituent is type I collagen. The remarkable tensile
strength of that protein is mainly down to its aminic bond.
Every third amino acid is glycine, and among the rest there
is a large fraction of proline or hydroxyproline. Unlike many
other proteins, type I collagen does not form an α-helix, but
rather combines three strands to form a triple helix. The formation starts with procollagen synthesis in the osteoblasts.
After exocytosis, a polypeptide is cleaved off the C-terminus
5
The so-called callus, which bridges the gap in fracture healing, is,
anatomically speaking, made up of woven bone, as is the microcallus
sometimes seen in trabecular bone.
6
Bone can be demineralized in vitro by acid or chelating agents. It is important
to realize that genuine demineralization does not occur in vivo. Rather, bone
resorption encompasses simultaneous demineralization and degradation of the
organic phase (see Section 1.3.3.1). It is therefore inappropriate to apostrophize
bone resorption, or even bone loss, as ‘demineralization’, as is sometimes done
in the literature.
7
This can be done by ‘ashing’ it at 500 °C.
c03.indd 31
31
2
4
1
1
2
4
Figure 1.3.3 Compact bone tissue. (a) Undecalcified section of
human compact bone after fuchsin staining. Transmitted light
microscopy with 100x magnification. Haversian systems, also called
secondary osteons, can be recognized by the surrounding cement line
(bright). Importantly, there are only a few osteocytic connections
across the cement line. The Haversian canal in their centre constitutes
a conduit for arterial, venous and nerve supply. The dense network of
canaliculi between the osteocytes can be appreciated, as well as the
concentric organization of their cell bodies around the Haversian
canal. (b) Schematic of the same slide as (a), with an analysis of the
overlapping of different Haversian systems in order to reveal the
tissue’s history. In this slide, osteons delineated with smaller numbers
are older than those delineated with larger numbers. When deciding
which osteon is older and which younger, the continuity of aligned
osteocytes is a key criterion. Sometimes, intracortical remodelling
leaves ‘chunks’ of bone behind that have no connection to a
Haversian or a Volkmann canal. These bits are referred to as
‘interstitial lamellae’ (marked by ‘x’). Apparently, the osteocytes
contained in them are derived from the dense canalicular network of
the Haversian system. There seems to be an accumulation of linear
microcracks within interstitial bone (Diab and Vashishth, 2007),
which pinpoints the crucial role that osteocytic communication may
play in the targeting of remodelling. Moreover, linear microcracks are
more detrimental to the risk of fracture than the diffuse microdamage
that is prevailing in other parts of bone and in the young (Diab et al.,
2006). It may therefore be that lack of remodelling of interstitial bone
is a key factor in osteoporotic fractures
10/18/2010 5:11:17 PM
32
SECTION 1
STRENGTH AND CONDITIONING BIOLOGY
and from the N-terminus to generate tropocollagen. This is
then enzymatically incorporated into the existing tropocollagen
network by so-called cross-links. In addition to enzymatic
cross-linking, which is a physiological process, there is also
non-enzymatic cross-linking by advanced glycation endproducts (AGEs). AGE cross-linking reduces a material’s
toughness (Garnero et al., 2006; Wang et al., 2002). It becomes
increasingly prevalent with age (Saito et al., 1997) and also
in bone with osteoporotic fractures (Saito et al., 2006; Shiraki
et al., 2008). It therefore seems possible that reduced toughness by AGEs is a contributing mechanism to osteoporotic
fractures.
Most of the mineral (= inorganic) phase consists of a tertiary
calcium phosphate crystal that is stoichiometrically similar to
hydroxyl apatite. However, in about 5% of the crystals the
phosphate group is replaced by carbonate, and the calcium can
also be replaced by sodium, potassium and other cations. We
should therefore speak of ‘bone apatite’. The high-order
elements in the inorganic phase cause considerable X-ray attenuation. X-ray-based methods have therefore become a standard
method of assessing the bone mineral.8 However, not all of the
bone mineral is crystalline, and there is a narrow seam along
the osteocytic canals that can readily exchange fluids and ions
(Arnold, Frost and Buss, 1971).
1.3.3
BONE BIOLOGY
Bone, at the material, tissue and organ levels, is generated and
maintained by four different kinds of cell. Osteoblasts can generate bone material and osteoclasts destroy it. Osteoblasts
derive either from bone marrow stromal cells (Aubin and Liu,
1996) or through transdifferentiation from the lining cells that
cover most bone surfaces. When forming bone, some of the
osteoblasts end-differentiate into osteocytes, which reside deep
within the bone (see Figures 1.3.3 and 1.3.4). When becoming
quiescent, osteoblasts reduce their height and differentiate back
into lining cells to stop bone formation altogether.
1.3.3.1
Osteoclasts
The term ‘osteoclast’ derives from the Greek words for ‘bone’
and ‘broken’. In fact, these cells degrade, dissolve and resorb
bone material. They do so in a tightly sealed extracellular space
that isolates the ‘osteolytic cocktail’ (Teitelbaum, 2000). This
cocktail contains H+ and proteolytic enzymes (e.g. collagenases,
cathepsins), which together erode the surface. Transcytosis
takes the solutes from the sealed zone to the basolateral domain
into a venole adjacent to the osteoclast. The void space, resulting from an osteoclast’s ‘bite’, is called a Howship lacuna, and
surface erosion by osteoclasts generates a scalloped surface
that can be thought of as a concatenation of such lacunae (see
Figure 1.3.4).
8
c03.indd 32
Hence the terms ‘bone mineral content’ and ‘bone mineral density’.
Scalloped
surface
Osteblasts
Osteoid seam
Osteocytes
Marrow
Bone
100 µm
Figure 1.3.4 Trabecular bone tissue. Undecalcified human trabecular
bone from the iliac crest in an eight-year-old boy. Goldner trichrome
staining and transmitted light microscopy (100×). The reader is kindly
asked to first look at the figure in a systematic way; that is, from
greater distance. You will then see that there are two darker surfaces
located on ‘top’ of a trabeculum, and two scalloped surfaces at its
‘bottom’. The dark surfaces consist of osteoid, which has recently
been laid down by the osteoblast arrays. The scalloped surfaces, on
the other hand, have undergone resorption. Together, resorption at the
bottom and formation at the top engender a drift of the bone structure
towards the top. This is typical of modelling. In this case the ‘top’ is
the external aspect of the os ileum, and the modelling drift will
mediate enlargement of the pelvis during growth. Note that bone
formation takes place on a smooth surface (that is, one that has not
yet undergone resorption), hence we can be sure that we are dealing
with modelling and not remodelling. Note also that the bone lamellae
(visible by the bright streaks) have variable orientation throughout the
section. Slide by courtesy of Rose Travers and Frank Rauch
The more active osteoclasts are, the more nuclei they
have. The average lifespan of an osteoclast is 12 days (Parfitt
et al., 1996), after which the cell undergoes apoptosis.
Osteoclasts have receptors and respond to parathyroid hormone,
calcitonin and interleukin 6. In vitro studies suggest that
osteoclasts are activated by receptor activator of nuclear factor
κ B (RANK), released by osteoblasts, which interacts with
RANK-ligand (RANKL) expressed on the osteoclasts’ membrane. Osteoprotegerin (OPG) is a decoy RANK receptor
expressed by osteoblasts which inhibits osteoclast differentiation and activity.
1.3.3.2 Osteoblasts
The term ‘osteoblast’ derives from the Greek for ‘bone’
and ‘germ’. Osteoblasts bear some similarity with fibroblasts
in that they generate collagen to enhance the extracellular
matrix. However, it is the privilege of the osteoblasts to induce
mineralization of that collagenous tissue to form bone material.
Naturally, this can take place only on existing bone surfaces.
For some reason, osteoblasts never work in isolation but rather
in conjunction with many other cells (see Figure 1.3.4). As
10/18/2010 5:11:17 PM
CHAPTER 1.3
stated above, osteoblasts can differentiate back and forth into
lining cells. They can also transdifferentiate into osteocytes, but
not back again.
The process of bone formation involves two steps. First, a
mix of different proteins, the so-called osteoid, is laid down.
This osteoid consists of collagen (>90%), elastine and glycosaminoglykanes; proteins with mechanical competence. In
addition to these, other proteins such as TGF-ß, osteocalcin and
osteopontin, which may have a regulatory function, are also
involved. The second step is the mineralization of the osteoid.
This seems to take around 10 days to begin (so-called mineralization lag time). Osteoblasts are involved in this process too,
providing the enzymes required (e.g. alkaline phosphatase and
osteocalcin). After this initiation, bone mineralization continues
more or less automatically. Importantly, crystallized apatite can
only be resolved by resorption. Hence, older bone material has
a greater concentration of minerals than younger material.
1.3.3.3
Osteocytes
Osteocytes reside deep within the bone tissue. They must rely
upon diffusion for exchange of nutrients and gases. To this end,
each osteocyte entertains 60 dendritic connections (Boyde,
1972) running through the so-called ‘canaliculi’ (see Figure
1.3.3). The volume required for this network and also for the
lacunae housing the osteocytes’ cell bodies amounts to approximately 2% of the total bone volume (Frost, 1960).
It is thought that osteocytes help to control the trafficking of
noncrystalline bone mineral (Talmage, 2004; Talmage et al.,
2003). Osteocytes possess receptors specific to parthyroid
hormone (PTH) (Divieti et al., 2001), suggesting that these cells
may respond to endocrine signals and thus mediate serum
calcium homoeostasis.
Osteocytes, lining cells and osteoblasts are all interconnected via connexons (gap junctions), forming a functional
syncytium that even extends into the stromal cells in the marrow
(Palazzini et al., 1998; Palumbo et al., 1990, 2001). It is very
likely that this osteocyte network constitutes a means of communication and information processing (see Section 1.3.5.4).
1.3.4
1.3.4.1
MECHANICAL FUNCTIONS
OF BONE
Material properties
Bone material is superior to all other materials of the human
body in terms of elasticity, strength and toughness.9 Figure 1.3.5
illustrates what these terms mean. As shown in the figure,
increases in strain and in stress are related. Strain is a measure
of the material’s deformation, and stress is the tension (force
per unit area) generated by the strain. There are two different
regions to be discerned in the diagram. Within the so-called
9
With the exception of teeth.
c03.indd 33
BONE PHYSIOLOGY
33
Stress-Strain Diagram
Yield
Point
250
Elastic
Plastic
Ultimate
Strength
200
150
100
Δσ
50
0
Δε
0
5000
10000
15000
20000
Strain [microstrain]
Figure 1.3.5 Stress–strain diagram. Strain (that is, deformation of a
solid material) is quantified by the dimensionless number ε. One
microstrain is deformation by 10−6 of the original length. Within the
material, the strain causes a stress (σ). This is given as force per unit
area. Two different portions can be discerned in the curve, one in
which strains are elastic (i.e. the energy is stored and returned) and
one in which they are plastic (i.e. the strain energy is not returned, but
rather transformed into material damage and heat). Young’s modulus
is given as E = Δσ/Δε in the elastic region of the stress–strain curve.
The stress at which the material fails is also referred to as the
material’s ultimate strength. Values in this diagram denote typical
values for compact bone in line with its typical loading direction
elastic region (for strains below the yield point) energy is elastically stored. In the plastic region the material absorbs some of
the deformation energy. This is often in the form of material
microdamage.
The elastic modulus (also called Young’s modulus or material stiffness) is defined as the slope of the stress–strain curve
in the elastic region. Resilience is the material’s capacity to
elastically store energy; it is given by the area under the curve
within the elastic region. The ultimate strength of a material
is the stress at which it fails. The toughness of a material is
the total amount of energy it can store and/or absorb before
failure; it is given by the area under the curve of both the
elastic and the plastic regions. A brittle material is one with
small toughness.
When considering these relationships (shown in Figure
1.3.5), four points should be borne in mind. First, the elastic
modulus of bone material increases with strain rate (i.e. the
speed of deformation). Second, the elastic modulus increases
with the degree of mineralization (Currey, 1984). Third, bone’s
material properties are different when loaded in compression,
tension and shear. Bone’s ultimate strength, for example, is
180 MPa in compression, but only 130 MPa in tensile loading.
Finally, and most importantly, bone material is anisotropic.
For example, elastic modulus and ultimate strength are up to
four times greater when loaded along the lamellae than perpendicular to them (Liu, Weiner and Wagner, 1999; Liu,
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STRENGTH AND CONDITIONING BIOLOGY
Wagner and Weiner, 2000). Normally, the orientation of lamellae in cortical bone is in parallel with the bone’s main axis
and the anisotropic behaviour is therefore aligned to maximize
the whole bone’s strength. By contrast, in trabecular bone the
lamella can be at virtually any angle in relation to the trabeculum’s axis (see Figure 1.3.4). It is therefore difficult to predict
the mechanical behaviour of bone without a full account of
its anisotropy. Accordingly, the validity of finite-element
models based on microCT data, as used by some scientists, is
questionable.
Another important material property is that of resistance to
fatigue. In bone, for example, failure stress decreases from
180 MPa when loaded once to 140 MPa when loaded a thousand
times, and to below 100 MPa when loaded a million times
(Gray, 1974). This is explained by the accumulation of microdamage (Cotton et al., 2005). Functionally, this leads to reduced
stiffness, strength and toughness. In a homogeneous material,
such as steel, cracks tend to propagate by themselves once they
exceed a length typical for that material (=Griffith length). This
is usually not the case for composite materials, such as bone,
where crack propagation is inhibited by several mechanisms
(Peterlik et al., 2006). Bone therefore has comparatively greater
toughness and can accumulate more plastic strains before
failure.
Remodelling (see Section 1.3.5.2) is the physiological
process that helps to repair bone microdamage. Unfortunately,
this does not always work. Fatigue fractures10 occur in response
to repetitive loading, typically in military recruits and athletes.
It is thought that a chronic change in habitual loading patterns
leads to the generation of microdamage, which promotes
remodelling activity. The excavation of the damaged tissue
necessarily raises the stresses experienced nearby, which in turn
potentiates the generation of new microdamage, finally giving
rise to a positive feedback loop or a vicious circle. Material
fatigue may similarly be involved in osteoporosis (Burr et al.,
1997), as the increased risk of fracture in older age can only
partly be explained by reductions in bone mass (Johnell et al.,
2005; Kanis et al., 2007). Furthermore, microdamage accumulation with increasing age is well documented (Diab et al.,
2006; Li et al., 2005) and it is therefore logical to expect some
contribution towards fracture propensity in osteoporotic
patients.
The pertinent question now is how far bone’s material properties vary. As outlined above, bone becomes stiffer with
increasing mineralization. One might therefore expect increased
material stiffness in older age. However, this does not seem to
occur (Zioupos and Currey, 1998); rather, old people’s bones
are characterized by greater variation in their material properties and it is possible that this contributes to reduced toughness
(Zioupos and Currey, 1998). With the exception of genetic
disorders such as osteogenesis imperfecta (see Section 1.3.5.3),
and disregarding evolutionary specialization of hard tissues
such as antler, tooth and tusk, the material properties of humans
have to be considered as fairly constant within individuals. As
10
Fatigue fractures are sometimes also called stress fractures. This term is
misleading as all fractures involve some kind of mechanical stress.
c03.indd 34
a consequence, adaptation of bones (as organs) to environmental stimuli has to occur through structural adjustment.
1.3.4.2 Structural properties
There are three different ways in which force can act upon solid
materials, namely compression, tension and shear (see Figure
1.3.6a). In bending, there is a combination of compression (on
the concave side; see Figure 1.3.6c) and tension (on the convex
side). Moreover, due to Poisson’s effect (see Figure 1.3.6b),
there is tension and shear even in mere compressive (=uniaxial)
loading. Hence, in reality any force application will elicit all
three kinds of strain within a solid material.
Adaptation to compression and tensile loading occurs
through alteration of the cross-sectional area perpendicular to
the line of action. More precisely, structural strength is given
by the product of cross-sectional area and the material’s ultimate strength. Structural adaptation to bending is a bit more
complicated. As depicted in Figure 1.3.6c, a neutral plane exists
in the centre of a beam the length of which does not change
during bending. Accordingly, as there is no strain in this plane,
it does not generate any stress and therefore does not contribute
to the beam’s resistance to bending. Conversely, the strains
(a)
(b)
Poisson‘s effect
Compression
Tension
Shear
(c)
Bending
Figure 1.3.6 Illustration of the different ways in which forces can
act upon a material. Compression and tension are the uniaxial loading
patterns (a). However, even simple compression will cause a
cross-expansion, known as Poisson’s effect (b). Hence there are shear
strains even in uniaxial loading. Bending causes a complex strain
pattern (c). Note that the upper edge of the beam is shortened,
whereas the lower edge becomes longer. The neutral plane (dashed
line) does not change in length
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BONE PHYSIOLOGY
35
Table 1.3.1 Example of the structural properties in four different beams and in the human tibia. All have identical cross-sectional areas, and
thus also identical strength in compression and tension. Their strength in bending, which is given by the moment of resistance (W), varies among
the different structures. WX is the moment of resistance for bending around the horizontal axis, and WY is for bending around the vertical axis.
Because of its rotational symmetry, WX = WY for the cylinders. This is not the case for the rectangular cylinder. Moreover, W is greater when the
cylinder is hollow, just because the available material is distributed more ‘eccentrically’. Accordingly, a flagpole is well designed to resist
bending moments with wind from all directions. In this sense, the tibia can be regarded as a combination of a hollow cylinder (distributing its
material far from the central fibre) and a rectangular beam with some degree of rotational asymmetry. This asymmetry accounts for bending
moments introduced by the eccentric attachment of the calf musculature, which imposes considerable forces upon the tibia. Adapted from
Rittweger et al. (2000)
Full cylinder
Hollow cylinder
Square beam
Rectangular beam
Human tibia
Size
R = 1.13
h=b=2
A (cm2)
WY (cm3)
WX (cm3)
4
1.13
1.13
r = 0.65
R = 1.30
4
1.62
1.62
h = 2.42
b = 1.65
4
1.1
1.62
4
1.39
1.62
y
x
become increasingly larger towards the edges of the crosssection. More precisely, the contribution of any material particle
to the beam’s bending stiffness increases with the square of its
distance from the neutral plane. The mathematical construct
derived from this principle to quantify the rigidity in bending
is the axial moment of inertia (I) and the structural strength in
bending is given by the axial moment of resistance11(W).
In practice, structures are strong in bending when W is large;
that is, when there is much material located far away from the
neutral plane. This is illustrated in Table 1.3.1, in which the
principle capability of the tibia to resist bending moments is
documented.
Architects have developed the concept of ‘tensintegrity’
through imitation of nature. This approach reduces bending
loads and attempts to replace them with compressive and tensile
forces. However, this is not always entirely possible and bending
does occur to some extent in the musculoskeletal system
(Biewener et al., 1983; Hartman et al., 1984). Accordingly, our
bones are adapted to it (Rittweger et al., 2000).
1.3.5
ADAPTIVE PROCESSES IN BONE
The notion that bones are capable of adapting to varying environmental conditions is relatively new. Much of our current
understanding is owed to Harold M. Frost. Whilst previous
researchers had focussed mainly on the activity of specific cells,
that is osteoblasts and osteoclasts, Frost considered the interplay between these cells to account for adaptive processes in
11
Also known as the section modulus.
c03.indd 35
4
1.33
1.33
bone. Two kinds of such interplay can be discerned, namely
modelling and remodelling. Whilst modelling prevails before
puberty, bone turnover is mainly through remodelling during
the later stages of life. Yet modelling still occurs in old age
(Erben, 1996).
1.3.5.1 Modelling
Modelling can be compared to the work of a sculptor. It is
characterized by drifts (Frost, 1990). As exemplified in Figure
1.3.4, these drifts occur such that envelopes undergoing formation oppose other envelopes undergoing formation. As a result,
solid bone structures can change their shape gradually. For
example, longitudinal growth is associated with enlargement of
the outer (=periosteal) and inner (=endocortical) diameters in
the diaphysis, which involves formation on the periosteal and
resorption on the endocortical envelopes, together enlarging the
shaft diameter.
Typically modelling leads to accrual of bone material, and
it thus enforces a bone’s structure. However, modelling is not
a mere synonym for formation, as it employs both formation
and resorption. Modelling is also thought to optimize the structure of trabecular networks (Huiskes et al., 2000) and it can in
addition help to neutralize bone flexure after fractures (Frost,
2004).
1.3.5.2 Remodelling
Remodelling replaces old bone material with new material. It
thus prevents microdamage accumulation (Frost, 1960; Mori
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SECTION 1
STRENGTH AND CONDITIONING BIOLOGY
and Burr, 1993). The so-called ARF sequence of remodelling
consists of the Activation of osteoclasts, the Resorption of old
bone, and the Formation of new bone (Takahashi, Epker and
Frost, 1964). Bone remodelling is effectuated by so-called
basic multicellular units (BMU). These consist of a few osteoclasts, which resorb the old bone material at the front of the
BMU. An artery and two veins are linked to them for blood
supply.12 At the back of the BMU, the resorption cavity is
filled up with new bone material by a cluster of osteoblasts.
The entire ARF sequence is thought to take 90–120 days to
complete.
Remodelling can either be stochastic or targeted. Stochastic
remodelling is thought to serve calcium homoeostasis and is
spatially unspecific. Targeted remodelling, by contrast, is specifically induced by bone microdamage (Burr et al., 1985).
BMUs tunnel their way in line with the principal stress (Hert,
Fiala and Petrtyl, 1994), possibly attracted to their target by
osteocyte apoptosis (Martin, 2007) occurring ahead of the
BMUs (Burger, Klein-Nulend and Smit, 2003) but also within
the vicinity of recent microcracks (Follet et al., 2007; Noble
et al., 1997, 2003).
Once an osteoclast is activated, osteoblasts are recruited,
either from lining cells or from osteoblast progenitors, to travel
behind the osteoclast. It is thought by many authors that osteoblastic and osteoclastic activities within a BMU are coupled
to each other. This belief is based on in vitro studies showing
that bone residues emerging from osteoclastic resorption, such
as TGF-β (Pfeilschifter et al., 1990) and osteocalcin (Mundy
et al., 1982), constitute a stimulus of chemotaxis and of differentiation to osteoblasts. Osteoclasts, conversely, are thought
to be controlled by osteoblasts through RANK and OPG (see
Section 1.3.3.1). However, as pointed out by Gasser (2006), it
is questionable whether such osteoblast/osteoclast coupling
does occur in vivo, as bone resorption and formation within the
BMU are separated in space and time, so that it is difficult to
consider how any coupling might work in vivo. A much simpler
hypothesis proposes that bone formation within the existing
BMU is primarily controlled by mechanical strain (Huiskes
et al., 2000; Smit and Burger, 2000), for example via Sost/
sclerostin expression (see Section 1.3.5.4).
With some imagination, the history of the remodelling
sequence can be deciphered under the microscope (see Figure
1.3.3). In compact bone, it leads to the generation of secondary
osteons, also called the Haversian systems (Havers, 1691). The
BMU’s bone balance is normally slightly negative. More precisely, of the 0.5 mm3 bone turned over by each BMU, 0.003 mm3
or 0.6% remains void (Frost, 2004). However, that loss is
increased under disuse conditions and after menopause, when
it can be almost complete in extreme cases.
12
It should be noted that there is also a nerve fibre alongside the vessels in the
BMU. Evidence suggests that sympathetic nervous fibres modulate the effects
of mechanical stimuli upon the remodelling process, although it is currently
unknown what exactly these modulatory effects are (Marenzana and Chenu,
2008).
c03.indd 36
1.3.5.3 Theories of bone adaptation
Within the realm of zoology, bone strains seem to be limited to
about 2000 microstrains, with remarkable similarity across different species (Biewener, 1990; Biewener and Taylor, 1986;
Rubin and Lanyon, 1984). It is important to bear in mind that
bone material properties are very similar across species, too.
There seems to be an evolutionary design principle, therefore,
to adjust whole-bone stiffness to the mechanical forces exerted
upon it; in other words, form follows function (Thompson,
1917; Wolff, 1899).
However, bones are not only genetically adapted to fulfil
their mechanical role; physiological processes also allow adaptation of bone stiffness and strength to environmental changes.
In a classic experiment Rubin and Lanyon (1987) demonstrated
that application of strains above a certain level induces accrual
of bone tissue, whilst lack of such strains leads to bone loss.
This has been conceptualized in a number of feedback control
theories (Beaupre, Orr and Carter, 1990; Fyhrie and Schaffler,
1995; Huiskes et al., 2000), of which the mechanostat theory
(Frost, 1987b) is probably the most well-known. According to
that theory, bone accrual by modelling is induced when strains
are in excess of the minimal effective strain for modelling
(MESm; see Figure 1.3.7a). When strains remain below the
minimal effective strain for remodelling (MESr), conversely,
BMU-based remodelling is associated with increasingly negative bone balance, leading to removal of unnecessary bone. This
can be understood as a negative feedback control system,
helping to adapt bone stiffness and thus strength to variable
forces (see Figure 1.3.7b).
Whilst the mechanostat theory is intuitive as well as formal,
it leaves a couple of important aspects open, and it contradicts
some empirical findings. For example, it makes no assumption
about the nature or the number of strain cycles. Evidence,
however, suggests that strain rate affects bone adaptive processes independently of strain magnitude (Mosley and Lanyon,
1998). Moreover, the number of strain cycles seems to be
important (Qin, Rubin and McLeod, 1998) as a large number
of strain cycles with small magnitude may be as effective as a
small number of large-magnitude cycles (Rubin et al., 2001).
Another observation not explained by the mechanostat theory
is that bone losses phase out after three to eight years of complete immobilization (Eser et al., 2004; Zehnder et al., 2004).
To accommodate for this phenomenon, a theory of cellular
accommodation has been proposed (Schriefer et al., 2005),
which proclaims that both the rapidity and the magnitude of a
change are meaningful.
Notwithstanding whatever theory can best explain bone
adaptive processes, there are two intriguing clinical examples
to be discussed in this context. As mentioned above, osteogenesis imperfecta (OI) is a heritable disorder, characterized by
fragile bones and caused by various different mutations in the
gene coding for type-1 collagen. OI is associated with enhanced
mineralization of bone (Boyde et al., 1999), which leads to
greater elastic modulus (Weber et al., 2006). Therefore the same
stresses will cause smaller strains. Interestingly, patients with
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CHAPTER 1.3
BONE PHYSIOLOGY
37
a
Fracture
Pos.
+
Bone
Stiffness
Bone Balance
b
MESm
MESr
Force
Strain
Bone
Balance
+
0
Strain
Neg.
+
Remodelling
Lamellar drifts
Woven bone drifts
-
Modeling
Remodelling
Figure 1.3.7 Mechanostat theory. (a) Schematic according to the original proposal (Frost, 1987a, 2003). According to the theory, habitual
strains control modelling and remodelling. With strains above the MESr threshold, remodelling-related bone losses are minimized. Below MESr,
however, remodelling is associated with an increasingly negative bone balance. When strains exceed the MESm threshold, modelling is turned
on, leading to gains in lamellar bone (most typical in humans) or woven bone formation. (b) Representation as a negative feedback control
system. For example, an increase in habitual force will lead to positive bone balance, and thus enhanced bone stiffness. This in turn takes the
bone strains back to the set value. As a result, the bone adapts to the increased force. It is important to recognize that the strain is regulated to be
constant in this model. By convention, arrows ending in ‘+’ denote concordant effects, whilst ‘−’ denotes discordant effects
OI have reduced bone mass (Rauch and Glorieux, 2004).
X-linked hypophosphataemic rickets (XLHR) can be regarded
as the ‘contrary’ condition, with bone hypomineralization due
to excessive renal phosphorus excretion. Bone strains in this
condition will therefore be larger than normal. In line with
expectations, XLHR patients seem to have enhanced bone
mineral density and mass in their forearm and lumbar spine
(Oliveri et al., 1991; Shore, Langman and Poznanski, 2000).
Taken together, these observations do indeed suggest that
strain-related signals govern whole-bone stiffness and strength
(Rauch, 2006).
1.3.5.4
Mechanotransduction
Given the fundamental importance of strain-related signals for
bone, the question arises as to how these signals are converted
into biological information. This process is referred to as mechanotransduction. It comprises the ‘recognition’ of strains (or a
related signal) within the bone, their processing, and communication with the surface on which either formation or resorption is to take place.
Earlier studies have focussed on the direct effects of
mechanical strains on osteocytes. Stretch-related calcium influx
(Ziambaras et al., 1998) and its propagation through gap junctions in the osteocyte network is one possible mechanism.
Likewise, insterstitial fluid flow (IFF) in the canalicular system
c03.indd 37
could constitute an elegant mechanism to amplify mechanical
signals. Indeed, in vitro studies with cultured osteoblasts
suggest that the effect of IFF could be more important than
the strain signal itself (Owan et al., 1997). In addition, it has
to be considered that IFF carries ions that give rise to piezoelectric and electrokinetic potentials (Guzelsu and Regimbal,
1990; Walsh and Guzelsu, 1991). IFF effects are thought to
be further mediated by nitric oxide (Bacabac et al., 2004) and
prostaglandin deliberation (Jiang and Cheng, 2001) to stimulate
osteoblastic bone formation. Within the osteocyte, there is
accumulating evidence for an involvement of Sost/sclerostin
expression (Robling et al., 2008), which in turn impinges on
osteoblastic bone formation, probably via LRP5/Wnt signalling
pathways.
In conclusion, science has started to unravel the events
involved in bone mechanotransduction. The question therefore
is how the different mechanisms found to be responsive to
strains interact. As highlighted by Harold Frost (1993), the
phenomenon of ‘flexure neutralization’ cannot be explained
by a single mechanotransductive mechanism. To solve this
problem, a ‘three-way rule’ considers local strains and the
whole-bone deformation. In support of such an explanation, the
marrow cavity seems to be an ideal candidate for discerning
whole-bone compression from whole-bone elongation. Indeed,
intramedullary hydraulic pressure oscillations (60 mmHg) have
been shown to prompt an increase in bone cross-section Qin
et al. 2003.
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38
SECTION 1
1.3.6
1.3.6.1
STRENGTH AND CONDITIONING BIOLOGY
ENDOCRINE INVOLVEMENT
OF BONE
Calcium homoeostasis
Of the 1–2 kg of calcium in the human body, only 1 g resides
outside the bones. The skeleton constitutes a large reservoir
with the theoretical potential to overwhelm the body with
calcium. Proper regulation of calcium fluxes into and out of
bone is therefore paramount to the milieu intérieur.
In mammals, the key players in the regulation of calcium
homoeostasis are vitamin D and its derivatives, as well as parathyroid hormone (PTH).13 PTH is secreted into the blood from
the parathyroid glands. PTH induces tubular reabsorption of
calcium and excretion of phosphorus, as well as D-hormone
synthesis in the kidney. It has no direct effect upon intestinal
absorption of calcium. However, PTH does promote renal
production of D-hormone, which in turn enhances intestinal
calcium absorption. Chronically elevated PTH levels favour
bone resorption, but bone formation can outweigh bone resorption when PTH levels peak intermittently. This engenders de
novo bone formation (Reeve et al., 1980), most likely through
modelling (Gasser, 2006). Consequently, recombinant PTH is
given to enhance bone mass and strength in patients with osteoporosis (Neer et al., 2001; Reeve, 1996). Calcitonin acts
antagonistically to PTH, but seems to be less important for the
control of calcium homoeostasis in mammals.
Vitamin D (cholecalciferol) is derived from nutritional
intake (Holick, 2005), and more importantly14 from UV lightinduced production in the skin from 7-dehydroxycholesterin. It
is transformed in two enzymatic steps in the liver and in the
kidney into the D-hormone (1,25-hydroxy-cholecalciferol).
D-hormone is an antagonist to PTH in some sense, as it inhibits
formation of PTH in the parathyroid glands. On the other hand,
D-hormone stimulates the uptake of calcium in the intestine and
kidney, and it also fosters bone mineralization. Besides its
effects upon calcium-controlling organs, vitamin D and its
derivatives have effects upon many other organs and cells in the
human body, including skeletal muscle and the breast glands.
It is important to realize that bone formation and resorption
are relatively slow instruments for the government of calcium
homoeostasis. For example, it takes 10 for osteoclast recruitment takes 8 days (Eriksen, Axelrod and Melsen, 1994). It
therefore seems that more rapid mechanisms are required for
an accurate control of calcium homoeostasis (Borgens, 1984;
Parfitt, 2003).
Within the mineral phase, insolulubility of the apatite crystals causes a concentration gradient for ions between the extracellular fluid (ECF) and the crystalline phase. This drives
calcium out of the ECF and into the bone (Talmage et al., 2003).
13
Interestingly, fish do not have PTH and rely solely upon calcitonin for
regulation of calcium homeostasis.
14
The relative contribution of nutritional intake and endogenous vitamin D
generation depends upon latitude, skin exposure and nutrition, including
‘fortified’ processed foods, all of which vary largely around the globe.
c03.indd 38
Bone material therefore has to be considered primarily as a sink
rather than as a source for calcium. In order to counteract this
continuous ion efflux from the ECF (Rubinacci et al., 2000),
calcium is actively transported by the osteocyte-lining cell continuum from the bone material into the ECF (Marenzana et al.,
2005).
1.3.6.2 Phosphorus homoeostasis
The human body contains approximately 600 g of phosphorus,
85% of which is located within the bones. Phosphorus is
involved in many biochemical reactions and biological processes and its concentration within the cell is relatively high
(1–2 mM). Nutrition is normally rich in phosphorus and intestinal absorption is usually around 80%. Both intestinal absorption and renal reabsorption are controlled by D-hormone. Serum
levels of phosphorus can vary considerably, causing fluctuations of 1 mM in physiological stimuli such as ingestion of
carbohydrates. Although there are some endocrine disorders
that affect phosphorus homoeostasis, it is usually not as crucial
as calcium homoeostasis.
1.3.6.3 Oestrogens
The public is increasingly aware that menopause, and thus
oestrogen withdrawal, causes bone loss and subsequently osteoporotic fractures. Yet there is only an incomplete understanding of oestrogen’s effects upon bone, particularly in relation to
exercise. Oestrogens are a family of steroid hormones, the most
active compound of which is 17-β oestradiol (E2). They rapidly
diffuse through the cell membrane to bind to tissue-specific
intracellular receptors and to unfold their genomic effects.
There are two different oestrogen receptors, ER-α and ER-β,
which are thought to both be present in bone cells but to transmit different effects.
Ovariectomy in a rat is frequently used as a model to mimic
the effects of oestrogen withdrawal upon bone. It leads to the
depletion of the trabecluar bone compartment (Kalu et al.,
1991) and to endocortical resorption (Kalu et al., 1989), but
also to periosteal bone formation (Turner, Vandersteenhoven
and Bell, 1987). Consequently, postmenopausal women have
wider bones with reduced cortical area, but more-or-less preserved bending and torsional stiffness, as compared to premenopausal women (Ferretti et al., 1998). It is clear, therefore,
on an observational level, that women in their fertile period
have more bone mineral than is required for mechanical reasons,
and it seems likely that evolution has foreseen this as a necessary calcium reservoir for pregnancy and breast-feeding
(Schiessl, Frost and Jee, 1998).
There is currently no consensus regarding the involvement
of oestrogens and oestrogen receptors in the mechanical adaptation of bone. Stringent evidence has been put forward to suggest
that oestrogen suppresses any bone response to exercise
(Jarvinen et al., 2003). In stark contrast, other authors have
shown that ER-α receptors are essential mediators of the
10/18/2010 5:11:17 PM
CHAPTER 1.3
skeleton’s response to mechanical strains (Lee et al., 2003). In
further contrast, Hertrampf et al. (2007) propose that ER-α
mediates those effects of oestrogen upon bone that are independent of exercise, whilst the exercise effects are mediated via
ER-β.
However, there is a growing understanding that oestrogens
suppress osteocyte apoptosis, most likely by antioxidative
c03.indd 39
BONE PHYSIOLOGY
39
effects (Mann et al., 2007), and thus probably also the rate
of bone remodelling. This could also explain the generally
greater cortical bone mineral density observed in women
(Wilks et al., 2008). Finally, involvement of oestrogens and
androgens in the skeletal sexual dimorphism is more or less
well understood, and so is the role of E2 in growth-plate
closure.
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SECTION 1
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1.4
Tendon Physiology
Nicola Maffulli1, Umile Giuseppe Longo2, Filippo Spiezia2 and Vincenzo Denaro2, 1 Queen Mary University of
London, Centre for Sports and Exercise Medicine, Barts, Mile End Hospital, The London School of Medicine and
Dentistry, London, UK, 2 Campus Bio-Medico University, Department of Orthopaedic and Trauma Surgery, Rome,
Italy
1.4.1
TENDONS
Tendons are part of a musculotendinous unit; they transmit
forces from muscle to rigid bone levers, producing joint motion
and enhancing joint stability (Kvist, 1994), and are made of
connective tissue.
Tendons are subjected to high forces, their material proprieties are higher than muscles, and given their proprioceptive
properties, they help to maintain posture (Benjamin, Qin and
Ralphs, 1995). Loads make tendons more rigid, thus they
absorb less energy but are more effective at moving heavy loads
(Fyfe and Stanish, 1992). At low rates of loading, the tendons
are more viscous, absorbing more energy, and being less effective at moving loads (Fyfe and Stanish, 1992). Tendons concentrate the pull of muscle on a small area. Hence the muscle
can change the direction of pull and act from a distance.
Tendons also produce an optimal distance between the muscle
belly and the joint without requiring an extended length of
muscle between the origin and insertion. Tendons have a peculiar anatomy on which their physical properties depend
(Kastelic, Galeski and Baer, 1978).
The number, size and orientation of the collagen fibres, as
well as their thickness and internal fibrillar organization determine the strength of a tendon (Oxlund, 1986).
Collagen, glycosaminoglycans, noncollagenous proteins,
cells, and water are abundant in tendons (Longo, Ronga and
Maffulli, 2009a, 2009b). About 90–95% of the cellular elements of tendons are tenoblasts and tenocytes. These are aligned
in rows between collagen fibre bundles (Longo et al., 2008b).
Tenoblasts transform into mature tenocytes, and are highly
metabolically immature, spindle-shaped cells, with numerous
cytoplasmic organelles (Maffulli et al., 2008). Tenocytes
produce extracellular matrix proteins (Longo et al., 2007,
2008a, 2009).
Sports or work activity may modify the alignment of the
fibres of the tendon.
The majority of the tendon fibres run in the direction
of stress, with a spiral component. Some fibres may run
perpendicular to the line of stress (Jozsa et al., 1991). Fibres
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
c04.indd 45
with relatively small diameter can run the full length of a
long tendon (Kirkendall and Garrett, 1997); those with a
diameter greater than 1500 A may not extend the full length
(O’Brien, 2005). Tendons may be flattened or rounded. They
may be found at the origin, insertion or form tendinous intersections within a muscle. An aponeurosis is a flattened tendon,
consisting of several layers of densely arranged collagen fibres.
The fascicles are parallel in one layer but run in different
directions in adjacent layers. The interior of the tendon consists mainly of longitudinal fibrils, with some transverse and
horizontal collagen fibrils (Chansky and Iannotti, 1991).
Transmission and scanning electron microscopy demonstrate
that collagen fibrils are orientated longitudinally, transversely
and horizontally. Crossing each other, the longitudinal fibrils
form spirals and plaits (Chansky and Iannotti, 1991; Jozsa
et al., 1991).
Tendons may give rise to fleshy muscles: for example, the
semimembranous tendon has several expansions that form ligaments, including the oblique popliteal ligament of the knee and
the fascia covering the popliteus muscle.
Segmental muscles that develop from myotomes often have
tendinous intersections. In certain areas, each segment has its
own blood and nerve supply, as is the case for the rectus
abdominis, the hamstrings and the sterno-clido-mastoid.
Tendons which cross articular surfaces or bone may have
sesamoid bones, already present as cartilaginous nodules in the
foetus. There is occasionally a sesamoid in the lateral head of
the gastrocnemius (fabella), in the tibialis anterior, opposite the
distal aspect of the medial cuneiform, and in the tibialis posterior below the plantar calcaneo navicular ligament, the ‘spring
ligament’. The long heads of the biceps brachii, the FHL (flexor
hallucis longus) and the popliteus are perfect examples of how
the tendons may be intracapsular. In these cases, tendons are
surrounded by the synovial membrane of the joint, and this
membrane extends for a variable distance beyond the joint
itself.
When tendons pass over bony prominences or lie in grooves,
they may be covered by fibrous sheaths or retinacula to prevent
them from bowstringing when the muscle contracts. Otherwise
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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reflection pulleys may hold tendons as they pass over a curved
area.
Tendons may be enclosed in synovial membrane when they
run in fibro-osseous tunnels or pass under retinacula, the fascial
slings. A film of fluid separates two continuous, concentric
layers of the membrane. The visceral layer surrounds the tendon
and the parietal layer is attached to the adjacent connective
tissues. A mesotendon is present as a tendon invaginates into
the sheath.
In the fibro-osseous sheaths of the phalanges of the hand and
foot, the synovial folds are called the vincula longa and vincula
brevia. Vincula contain the blood vessels, which supply the
flexor tendons inside the sheaths. The lining of the sheath
secretes synovial fluid and is responsible for inflammatory reactions through cellular proliferation and the formation of more
fluid, which may result in adhesions and restriction of movement between the two layers.
The plantaris tendon in the gastrosoleus complex is a classic
example of supernumerary tendon.
1.4.2 THE MUSCULOTENDINOUS
JUNCTION
In the mesenchyme, tendons develop independently; their connection with the muscle appears later. The junctional area
between the muscle and the tendon is called the myotendinous
junction. During transmission of muscular contractile force to
the tendon, this area is subjected to great mechanical stress. The
collagen fibres of a tendon extend into the body of the muscle,
increasing the anchoring surface area. Tendinous fibres are disposed to direct the force produced by the muscular contraction
to the point of insertion.
The tendon elongates at the musculotendinous junction, and
the growth plate of a muscle is considered to be the musculotendinous junction. It contains cells that deposit collagen and
can elongate rapidly, and also contains nerve receptors and
organs of Golgi. Terminal expansions of muscle fibres may be
present here, as shown by electron microscopy. These ends
have a highly indented sarcolemma, with a dense internal layer
of cytoplasm into which the actin filaments of the adjacent
sarcomeres are inserted. Muscle tears tend to occur at the musculotendinous junction (Garrett, 1990). The sites of muscle
tears can be explained by variations in the extent of the tendon
into the muscle at the origin and insertion. The adductor longus
tendon may present variations in the shape and extent. In the
hamstrings, tendinous intersections denoting the original myotomes are found.
1.4.3
THE OSEOTENDINOUS
JUNCTION
The osteotendinous junction (OTJ) presents a gradual transition
from tendon to fibrocartilage to lamellar bone. This area can be
divided into four zones: pure fibrous tissue, unmineralized
fibrocartilage, mineralized fibrocartilage, and bone. The outer
c04.indd 46
limit of the mineralized fibrocartilage, the tidemark, consists of
basophilic lines (cement or blue lines). These lines are usually
smoother than at the osteo-chondral junction. On the tendon
side of the tidemark there are chondrocytes. Tendon fibres can
extend as far as the osteo-chondral junction. Rare blood vessels
may cross from bone to tendon. If the attachment is very close
to the articular cartilage, the zone of fibrocartilage is continuous
with the articular cartilage. The chemical composition of fibrocartilage is age-dependant, both in the OTJ and in other fibrocartilagenous zones of the tendon.
Smooth mechanical transition is allowed by osteogenesis at
the tendon–bone junction. The periosteum has osteogenic
potential, except where tendons are inserted. Dense collagen
fibres connect the periosteum to the underlying bone. During
bone growth, collagen fibres from the tendon are anchored
deeper into the deposited bone. In stress fractures of the tibia,
variations in hot spots on bone scans may be explained by variations in the attachments of the tendon to bone (Ekenman et al.,
1995).
The occupation and sports activity of an individual may
influence the structure of the attachment zone of a tendon. For
example, the insertion of the biceps of a window cleaner, who
works with his forearm pronated, will differ from that of an
individual who works with the forearm supinated.
1.4.4
NERVE SUPPLY
Sensory nerves from the overlying superficial nerves and from
nearby deep nerves supply the tendons. The nerve supply is
mostly, but not all, afferent. Afferent receptors can be found
near the musculotendinous junction (Stilwell, 1957), either on
the surface or in the tendon. Longitudinal plexus enter via the
septa of the endotendon or the mesotendon if there is a synovial
sheath. Branches may reach the surface or the interior of a
tendon, passing from the paratenon via the epitenon.
There are four types of receptor. Type I receptors (pressure
receptors or Ruffini corpuscles) are very sensitive to stretch and
adapt slowly (Stilwell, 1957). Type II receptors (Vater–Pacini
corpuscles), are activated by any movement. Type III receptors
(Golgi tendon organs) are mechanoreceptors. They consist of
unmyelinated nerve endings encapsulated by endoneural tissue.
They lie in series with the extra fusal fibres and monitor
increases in muscle tension rather than length. Muscle contraction produces pressure; the lamellated corpuscles respond to
this stimulus, with the amount of pressure depending on the
force of contraction. They may provide a more finely tuned
feedback. Type IV receptors are the free nerve endings that act
as pain receptors.
1.4.5
BLOOD SUPPLY
The blood supply of tendons is divided into three regions: (1)
the musculotendinous junction; (2) the length of the tendon; and
(3) the tendon–bone junction. The blood vessels originate from
vessels in the perimysium, periosteum and via the paratenon
and mesotendon.
10/18/2010 5:11:18 PM
CHAPTER 1.4
Superficial vessels in the surrounding tissues allow the
supply of blood to the musculotendinous junction. Small arteries branch and supply both muscles and tendons without anastamosis between the capillaries.
The paratenon is the main blood source to the middle portion
of the tendon. The main blood supply in tendons that are
exposed to friction and are enclosed in a synovial sheath is via
the vincula. Blood vessels in the paratenon run transversely
towards the tendon and branch several times before running
parallel to the long axis of the tendon. The vessels enter the
tendon along the endotendon; the arterioles run longitudinally,
flanked by two venules. Capillaries loop from the arterioles to
the venules, but they do not penetrate the collagen bundles.
Vessels supplying the bone–tendon junction supply the
lower third of the tendon. There is no direct communication
between the vessels because of the fibrocartilaginous layer
between the tendon and bone, but there is some indirect anastamosis between the vessels.
At sites of friction, torsion, or compression, the blood supply
of tendons is compromised; this happens in the tibialis posterior, supraspinatus, and Achilles tendons (Frey, Shereff and
Greenidge, 1990; Ling, Chen and Wan, 1990). In the critical
zone of the supraspinatus there can be an area of hypervascularity secondary to low-grade inflammation with neovascularization due to mechanical irritation (Ling, Chen and Wan, 1990).
There is an avascular region at the metacarpo-phalangeal
joint and the proximal interphalangeal joint, possibly resulting
from the mechanical forces exerted at these zones (Zhang et al.,
1990).
The Achilles tendon is the thickest and strongest tendon. It
is approximately 15 cm long and on its anterior surface it
receives the muscular fibres from the soleus for several centimetres. As the tendon descends, it twists; this produces an area
of stress in the tendon, which is most marked 2–6 cm above the
insertion, the area of poor vascularity, a common site of tendon
ailments (Barfred, 1971).
The blood supply of the Achilles tendon consists mainly of
longitudinal arteries that course the length of the tendon. This
tendon is supplied at its musculotendinous junction, along the
length of the tendon, and at its junction with bone.
1.4.6
COMPOSITION
Tendons consist of 30% collagen and 2% elastin embedded in
an extracellular matrix containing 68% water and tenocytes.
Elastin contributes to the flexibility of the tendon. The collagen
protein, tropocollagen, forms 65–80% of the mass of dryweight tendons and ligament.
Tendons are relatively avascular and appear white. A tendon
is a roughly uniaxial composite mainly comprising type I collagen in an extracellular matrix composed largely of mucopolysaccharides and a proteoglycan gel (Kastelic, Galeski and Baer,
1978).
Ligaments and tendons consist mainly of type I collagen.
Ligaments have 9–12% type III collagen and are more cellular
than tendons (Khan et al., 1999). Type II collagen is found
abundantly in the fibrocartilage at the attachment zone of the
c04.indd 47
TENDON PHYSIOLOGY
47
tendon (the OTJ) and is also present in tendons that wrap around
bony pulleys. Collagen consists of clearly defined, parallel, and
wavy bundles and has a characteristic reflective appearance
under polarized light between the collagen bundles.
1.4.7
COLLAGEN FORMATION
The structural unit of collagen is the tropocollagen. It is a long,
thin protein, 280 nm long and 1.5 nm wide, consisting mainly
of type I collagen. Tropocollagen is formed as procollagen in
fibroblast cells and is secreted and cleaved extracellularly.
Successively, it becomes collagen.
The α-chain comprises 100 amino acids. There are three
α-chains, which are surrounded by a thin layer of proteoglycans
and glycosaminoglycans Two of the α-chains are identical
(α1); one differs slightly (α2). The three-polypeptide chains
each form a left-handed helix. Hydrogen bonds connect the
chains together to form a rope-like right-handed superhelix. A
collagen molecule has a rod-like shape. Almost two thirds of
the collagen molecule consists of three amino acids, glycine
(33%), proline (15%), and hydroxyproline (15%). Each α-chain
consists of a repeating triplet of glycine and two other amino
acids. Glycine is found at every third residue, while proline
(15%) and hydroxyproline (15%) occur frequently at the other
two positions. Glycine enhances stability by forming hydrogen
bonds between the three chains. Collagen also contains two
amino acids, hydroxyproline and hydrozylysine (1.3%), which
are not often found in other proteins. Hydroxyproline and
hydroxylysine increase the strength of collagen. Hydroxyproline
is also essential in the hydrogen bonding between the polypeptide chains, while hydroxylysine is essential in the covalent
cross-linking of tropocollagen into bundles of various sizes.
The domains are non-helical peptides placed at both ends of
procollagen. Peptides enzymatically cleave the domains to form
tropocollagen.
1.4.8
CROSS-LINKS
Electrostatic cross-linking chemical bonds stabilize tropocollagen molecules and hold them together. Hydroxyproline is
important in hydrogen bonding (intramolecularly) between the
polypeptide chains. Hydroxylysine is also involved in covalent
(intermolecular) cross-linking between adjacent tropocollagen
molecules. Lysyl-oxidase is the key enzyme; it is a rate-limiting
step of collagen cross-linking. Cross-links of hydroxylysin are
the most prevalent intermolecular cross-links in native insoluble collagen, and have a paramount role in creating the tensile
strength of collagen, allowing energy absorption, and increasing collagen’s resistance to proteases.
Shortly after the synthesis of collagen, fibres acquire all the
cross-links they will have. Cross-links are at their maximum in
early postnatal life and reach their minimum at physical maturity. Newly synthesized collagen molecules are stabilized
by reducible cross-links, but their numbers decrease during
maturation. Non-reducible cross-links are found in mature collagen, which is stiffer, stronger, and more stable. Reduction of
10/18/2010 5:11:18 PM
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STRENGTH AND CONDITIONING BIOLOGY
cross-links makes collagen fibres weak and friable. Hence,
cross-linking of collagen is one of the best biomarkers of
ageing.
Cross-linking substances are removed by metabolic processes in early life but accumulate in old age.
1.4.9
ELASTIN
Elastin does not contain much hydroxyproline or lysine, but is
rich in glycine and proline. It does not form helices and is
hydrophobic. It has a large content of valine and contains
desmosine and isodesmonine, which form cross-links between
the polypeptides, but no hydroxylysine. Elastin contributes to
the flexibility of a tendon.
1.4.10
CELLS
Tenocytes and tenoblasts or fibroblasts are tendon cells.
Tenocytes are flat, tapered cells, spindle-shaped longitudinally
and stellate in cross-section. Tenocytes may be found sparingly
in rows between collagen fibrils. They posses cell processes that
form a three-dimensional network extending through the extracellular matrix. The communication is via cell processes, and
these cells may be motile (Kraushaar and Nirschl, 1999).
Tenoblasts are spindle-shaped or stellate cells with long
tapering eosinophillic flat nuclei. Tenoblasts are motile and
highly proliferative. They have well-developed rough endoplasmic reticulum, on which the precursor polypeptides of collagen,
elastin, proteoglycans, and glycoproteins, are synthesized.
Tendon fibroblasts (tenoblasts) in the same tendon may have
different functions. The epitenocyte functions as a modified
fibroblast with a well-developed capacity of repair.
1.4.11
GROUND SUBSTANCE
Ground substance is composed of proteoglycans and glycoproteins which surround the collagen fibres. Gliding and crosstissue interactions are allowed by the high viscosity of ground
substance, which provides the structural support, lubrication,
and spacing of the fibres. Nutrients and gases diffuse through
ground substance. It regulates the extracellular assembly of
procollagen into mature collagen. Water makes up 60–80% of
its total weight. Less than 1% of the total dry weight of tendon
is composed of proteoglycans and glycoproteins. These proteins
are involved with intermolecular and cellular interactions and
maintain the water within the tissues. Proteoglycans and glycoproteins also play an important role in the formation of fibrils
and fibres. The covalent cross-links between the tropocollagen
molecules reinforce the fibrillar structure.
The water-binding capacity of these macromolecules is
important. Most proteoglycans are orientated at 90° to collagen,
and each molecule of proteoglycan can interact with four collagen molecules. Others are randomly arranged to lie parallel
c04.indd 48
to the fibres, but they only interact with one fibre (Scott, 1988).
The matrix is constantly being turned over and remodelled by
the fibroblasts and by degrading enzymes (collagenases, proteoglycanase, glycoaminoglycanase, and other proteases).
The proteogylcans and glycoproteins consist of two components, glycosaminogylcans (GAGs) and structural glycoproteins. The main proteogylcans in tendons associated with
glycosaminoglycans are dermatan sulfate, hyaluronate, chondroitin 4 sulfates, and chondroitin 6 sulfates. Other proteoglycans found in tendons include biglycan, decorin, and aggrecan.
Aggrecan is a chondroitin sulfate bearing large proteoglycan in
the tension regions of tendons (Vogel et al., 1994). The glycoproteins consist mainly of protein, such as fibronectin, to which
carbohydrates are attached.
Fibronectins are high-molecular weight noncollagenous
extracellular glycocoproteins. Fibronectin plays a role in cellular adhesion (cell–cell and cell–substrate) and cell migration.
It may be essential for the organization of collagen I and III
fibrils into bundles, and may act as a template for collagen fibre
formation during the remodelling phase.
Hyaluronate is a high-molecular weight matrix glycosaminoglycan, which interacts with fibronectin to produce a
scaffold for cell migration. It later replaces fibronectin.
Integrins are extracellular matrix-binding proteins with specific cell-surface receptors. Large amounts of aggrecan and
biglycan develop at points where tendons wrap around bone and
are subjected to compressive and tensional loads. TGF-β may
be involved in differentiation of regions of tendon subjected to
compression as compressed tendon contains both decorin and
biglycan, whereas tensional tendons contain primarily decorin
(Vogel and Hernandez, 1992). The synthesis of proteoglycans
begins in the rough endoplasmic reticulum, where the protein
portion is synthesized. Glycosylation starts in the rough endoplasmic reticulum and is completed in the Golgi complex,
where sulfation takes place. The turnover of proteoglycans is
rapid, from 2 to 10 days. Lysosomal enzymes degrade the proteoglycans, and lack of specific hydrolases in the lysososmes
results in their accumulation.
When newly formed, the ground matrix appears vacuolated.
The formation of tropocollagen and of extracellular matrix are
closely inter-related. The proteoglycans in the ground substance
seem to regulate fibril formation as the content of proteoglycans
decreases in tendons when the tropocollagen has reached its
ultimate size. An adequate amount of ground substance is necessary for the aggregation of collagenous proteins into the shape
of fibrils.
1.4.12
CRIMP
Crimp represents a regular sinusoidal pattern in the matrix.
Collagen fibrils in the rested, nonstrained state are not straight,
but wavy or crimped. Both tendons and ligaments have the
main feature of crimp. The periodicity and amplitude of crimp
is structure-specific (Viidik, 1973). It is visualized under polarized light. Crimp provides a buffer in which slight longitudinal
elongation can occur without fibrous damage, and acts as a
10/18/2010 5:11:18 PM
CHAPTER 1.4
shock absorber along the length of the tissue. Different patterns of crimping exist: straight or undulated in a planar wave
pattern.
The fibre bundles are interwoven without regular orientation
and the tissues are irregularly arranged. Fibres are regularly
arranged and have an orderly parallel arrangement if tension is
only in one direction. The parallel orientation of collagen fibres
is lost in tendinopathy. A decrease in collagen fibre diameter
and in the overall density of collagen may be found. Collagen
microtears may be surrounded by erythrocytes, fibrin, and
fibronectin deposits. In a normal tendon, collagen fibres in
tendons are tightly bundled in a parallel fashion. In tendinopathic samples there is unequal and irregular crimping, loosening, and increased waviness of collagen fibres, with an increase
in type III (reparative) collagen.
Many factors can affect collagen production: heredity, diet,
nerve supply, inborn errors, and hormones. Corticosteroids also
inhibit the production of new collagen. Insulin, oestrogen, and
testosterone may increase collagen production.
Osteogenesis imperfecta, Ehlers–Danos syndrome, scurvy,
and progressive systemic sclerosis are collagen disorders.
Muscles and tendons atrophy and the collagen content decreases
when the nerve supply to the tendon is interrupted. Inactivity
also results in increased collagen degradation, decreased tensile
strength, and decreased concentration of metabolic enzymes.
Given the reduction of enzymes essential for the formation of
collagen with age, repair of soft tissue is delayed in the older
age groups. Exercise increases collagen synthesis, the number
and size of the fibrils, and the concentration of metabolic
enzymes. Physical training increases the tensile and maximum
static strength of tendons.
Cell and tissue organization, cell–cell and cell–matrix communication, cell proliferation and apoptosis, matrix remodelling, cell migration, and many other cell behaviours in both
physiological and pathophysiological conditions in all the musculoskeletal tissues (bone, cartilage, ligament, and tendon) are
modulated by dynamic stresses and strains.
Changes in tissue structure and function following application of mechanical forces, including gravity, tension, compression, hydrostatic pressure, and fluid shear stress are the main
subjects of mechanobiology (Wang, 2006). The ability of
tendons to alter their structure in response to mechanical loading
is called tissue mechanical adaptation, and it is effected by cells
in tissues at all times. It is not yet clear how cells perceive
dynamic stresses and strains and convert them into biochemical
signals which lead to tissue adaptive physiological or pathological changes.
Tendons show viscoelastic behaviour and adapt their functional and mechanical features to dynamic stresses and strains.
The mechanical behaviour of tendons is unique to their peculiar
structural characteristics. Viscoelasticity is the property of
materials that exhibit both viscous and elastic characteristics
when undergoing deformation (Butler et al., 1978). Collagen,
water, and interactions between collagenous proteins and
noncollagenous proteins (i.e. proteoglycans) determine the
viscoelastic features of tendons. Tendons are therefore more
deformable at low strain rates, but they are less effective in load
c04.indd 49
TENDON PHYSIOLOGY
49
transfer. Tendons are less deformable at high strain rates, with
high degree of stiffness, and they become more effective in
moving high loads (Jozsa and Kannus, 1997).
Structural changes in tendons are caused by dynamic stresses
and strains imposed on them. Sports determine an increase in
the cross-sectional area and tensile strength of tendons, and
tenocytes increase the production of type I collagen (Langberg,
Rosendal and Kjaer, 2001; Michna and Hartmann, 1989;
Suominen, Kiiskinen and Heikkinen, 1980; Tipton et al., 1975).
Inappropriate physical exercise or occupation leads to tendon
overuse injuries and tendinopathy (Khan and Maffulli, 1998;
Maffulli, Khan and Puddu, 1998). There is greater matrix–
collagen turnover in growing chickens, resulting in reduced
maturation of tendon collagen during high-intensity exercise
(Curwin, Vailas and Wood, 1988). In an animal model following high-intensity training there is an increased IGF-I immunoreactivity (Hansson et al., 1988). IGF-I acts as a potent
stimulator of mitogenesis and protein synthesis (Simmons et
al., 2002) and therefore may be used as a protein marker for
remodelling activities of the tendon.
Physical training results in an increased turnover of type I
collagen in local connective tissue of the peritendinous Achilles
tendon region (Langberg, Rosendal and Kjaer, 2001).
Immobilization decreases the total weight, tensile strength, and
stiffness of tendons (Maffulli and King, 1992).
Tendon overuse injuries (Amiel et al., 1982) are common
in occupational and athletic settings (Almekinders and Temple,
1998). An important causative factor for tendinopathy is excessive mechanical loading (Lippi, Longo and Maffulli, 2009).
Repetitive strains below the failure threshold of tendons may
cause microinjuries to the tendon, possibly with episodes of
tendon inflammation (Khan and Maffulli, 1998). Human
tendons following repetitive mechanical loading present
increased levels of PGE2 (Langberg, Rosendal and Kjaer,
2001). Studies show that in vitro repetitive mechanical loading
of human tendon fibroblasts increases the production of PGE2
(Almekinders, Banes and Ballenger, 1993) and LTB4 (Li et
al., 2004). Prolonged PGE1 administration produces peri- and
intra-tendinous degeneration (Sullo et al., 2001). Degenerative
changes within the rabbit patellar tendon have been reported
after repeated exposure of the tendon to PGE2 (Khan, Li
and Wang, 2005). Clinical studies have reported no significant
differences in the mean concentrations of PGE2 between
tendons with tendinopathy and normal tendons. However,
there were higher concentrations of the excitatory neurotransmitter glutamate in tendinopathic Achilles tendons (Alfredson,
Thorsen and Lorentzon, 1999). Repetitive submaximal strains
below failure threshold are probably responsible for tendon
microinjuries and episodes of PG-mediated tendon inflammation. It is therefore possible that when microinjuries become
clinically evident, the PGEs are no longer present in the
tendon.
Overuse of tendons can lead to detrimental changes in
tendon tissue structure and result in tendinopathic changes
(Longo et al., 2007, 2008a, 2009). Despite the clear clinical
relevance of mechanotransduction signalling pathways in tenocytes, the mechanisms by which these cells perceive and
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50
SECTION 1
STRENGTH AND CONDITIONING BIOLOGY
respond to mechanical stimuli are poorly understood. Calcium
ions play an important role in mechanotransduction and act as
one of the primary second messengers utilized by cells to
convert mechanical signals to biochemical signals (Bootman
et al., 2001). Preliminary data have shown upregulation of
calcium signalling pathways in human tenocytes exposed to
fluid flow-induced shear stress (el Haj et al., 1999), and it has
been proposed that mechanosensitive and voltage-gated ion
channels may play a key role in the initial responses of human
tenocytes to mechanical load (Banes et al., 1995). Both mechanosensitive and voltage-gated ion channels may have key roles
in mechanotransduction signalling pathways in their connective
tissues, including bone (el Haj et al., 1999), smooth muscle
(Holm et al., 2000), and heart cells (Niu and Sachs, 2003).
Voltage-operated calcium channels (VOCCs) permit the influx
of extracellular calcium in response to changes in membrane
potential and form the basis of electrical signalling in excitable
cells (Catterall, 2000). VOCCs also are potentially mechanosensitive (Lyford et al., 2002). Mechanosensitive members of
the tandem pore domain potassium channel family (Patel and
Honore, 2001), including TREK-1 and TREK-2, may be
c04.indd 50
involved in mechanotransduction signalling pathways in
smooth-muscle cells (Koh et al., 2001), heart cells (Aimond et
al., 2000), and bone cells (Hughes et al., 2006). TREK-1 channels produce a spontaneously active background leak potassium
conductance to hyperpolarize the cell membrane potential and
regulate electrical excitability (Heurteaux et al., 2004). TREK-1
is sensitive to membrane stretch, lysophosphatidylcholines,
lysophosphatidic acids, polyunsaturated fatty acids, intracellular pH, temperature, and a range of clinically relevant compounds including general and local anaesthetics (Gruss et al.,
2004).
Human tenocytes express a diverse array of ion channels,
including L-type VOCCs and TREK-1 (Magra et al., 2007).
VOCCs are likely to be a key mediator of calcium signalling
events in human tenocytes, whereas TREK-1 could potentially
perform a number of roles in tenocytes, ranging from osmoregulation and cell volume control, to control of resting membrane
potentials levels of electrical excitability, to the direct detection
of mechanical stimuli. TREK-1 and VOCC channels could be
potential targets for pharmacological management of chronic
tendinopathies (Magra et al., 2007).
10/18/2010 5:11:18 PM
CHAPTER 1.4
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1.5
Bioenergetics of Exercise
Ron J. Maughan, School of Sport, Exercise and Health Sciences, Loughborough University, Loughborough, UK
1.5.1
INTRODUCTION
All life requires the continuous expenditure of energy. Even at
rest, the average human body consumes about 250 ml of oxygen
each minute; this oxygen is used in the chemical reactions that
provide the energy necessary to maintain physiological function. During exercise, the muscles require additional energy to
generate force or to do work, the heart has to work harder to
increase blood supply, the respiratory muscles face an increased
demand for moving air in and out of the lungs, and the metabolic rate must increase accordingly. In sustained exercise, an
increased rate of energy turnover must be maintained for the
whole duration of the exercise and for some time afterwards;
depending on the task and the fitness level of the individual,
this may be from 5 to 20 times the resting metabolic rate. In
very high-intensity activity, the demand for energy may be
more than 100 times the resting level, though such intense
efforts can be sustained for only very short periods of time.
These observations immediately raise several questions: what
is this energy used for, where does it come from, what happens
when the energy demand exceeds the energy supply, and more.
Though technically it belongs in the field of exercise biochemistry, an understanding of fuel consumption and the processes involved in energy supply is fundamental to exercise
physiology and sports nutrition.
1.5.2
EXERCISE, ENERGY, WORK,
AND POWER
As mentioned above, the energy demand of the resting metabolism of the average human is met by a rate of oxygen consumption of about 250 ml/min. At rest, the body is in a relative steady
state, at least with regard to oxygen content, and all of the
energy is supplied by oxidative metabolism, though there will
be energy supply that does not involve oxygen consumption in
some tissues. The oxygen consumption and the energy expenditure therefore tally very closely; they are in effect different ways
of expressing the same thing. In some tissues, however, energy
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
c05.indd 53
is generated without oxygen being consumed. Red blood cells
do not have any mitochondria; these are the subcellular structures that house the metabolic machinery which allows energy
to be derived from metabolic fuels in the presence of oxygen.
Red blood cells meet their energy needs by breaking down
glucose to lactate in a series of reactions that do not involve
oxygen. Other tissues, however, remove that lactate from
the bloodstream, either by using it as a fuel in the presence
of oxygen or by converting it to other valuable metabolic
compounds.
In some forms of exercise, not all of the energy demand is
met by oxidative metabolism. The rate of oxygen consumption
increases more or less linearly as the power output increases,
but there is a finite limit to the amount of oxygen that an individual can use: this is identified as the maximum oxygen uptake,
or VO2max, and is discussed further below. An individual’s
VO2max is often referred to as their aerobic capacity and is one
of the defining physiological characteristics. Human skeletal
muscle, however, can perform work in the absence of an adequate supply of oxygen as a consequence of its ability to generate energy without any oxygen consmuption. In these situations,
other ways of expressing the metabolic rate must be used. An
oxygen consumption of 250 ml/min is equivalent to an energy
expenditure of about 5 kJ/min (or about 1.3 kcal/min for those
who use the calorie, as many nutritionists do). A rate of energy
expenditure is an expression of power, and the SI unit of power
is the Watt (W), which is equal to 1 J/s; 5 kJ/min is therefore
equivalent to about 83 W (Winter and Fowler, 2009). Oxidation
of carbohydrate generates about 5 kcal for each litre of oxygen
consumed; the corresponding figure when fat is the fuel is about
4.7 kcal. A 70 kg runner moving at a speed of 15 km/h will
require about 3.5 l of oxygen per minute, or about 1.17 kW. It
is important to recognize, however, that not all muscular activity, and therefore not all energy expenditure, relates to the
performance of external work that can be measured, though it
does require an input of chemical energy.
It is often convenient to think of rates of energy expenditure
in terms of the amount of oxygen that would have to be consumed if all of the energy demand were to be met by energy
generated by oxidative metabolism. It is important, too, to
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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recognize that many of the physiological responses to exercise
are proportional not to the rate of oxygen uptake (or the rate of
power output), but rather to the energy demand as a fraction of
the individual’s aerobic capacity. A survey of a large and
diverse sample population will show little correspondence
between heart rate and power output during a cycle ergometer
test, for example. The relationship will be just the same if
oxygen uptake is substituted for power output. Recalculating
the data, however, will show a relatively good relationship
between heart rate and the fraction of aerobic capacity that is
employed. The energy demand will be very similar for all individuals at the same power output, but the physiological
responses will be very different.
When energy is required by the body, it is made available
by the hydrolysis of the high-energy phosphate bonds in the
adenosine triphosphate (ATP) molecule. Storage of ATP in
substantial amounts is not possible – the amount of chemical
energy stored in each molecule of ATP is rather small and it
would be inefficient to store more because of the mass that
would have to be carried. All of the body’s energy-supplying
mechanisms are geared towards the resynthesis of ATP;
although the ATP concentration within the cell remains almost
constant, this is only because the rates of breakdown and resynthesis are balanced. The greater the energy demand, the faster
the turnover rate. The amount of energy released by hydrolysis
ATP is about 31 kJ per mole of ATP. Given that the molecular
weight of ATP is about 507, we can calculate that a resting
individual with an energy turnover of 83W (which is 83 J/s)
must be breaking down about 1.4 g of ATP every second. As
the ATP concentration in the cells remains constant, enough
energy must be fed back into the system to regenerate ATP at
precisely the same rate. Our runner in the example above must
break down about half a kilogram of ATP every minute to
maintain her pace. Given that the total ATP content of the body
is about 50 g, this means that each molecule of ATP in the body
turns over on average about once every six seconds.
Ensuring that this energy is made available at exactly the
rate it is required is one of the major challenges to the body
during exercise.
1.5.3
SOURCES OF ENERGY
All of the energy used by the human body is ultimately derived
from the chemical energy in the foods that we eat. This chemical energy may be used immediately, or it may be stored
(primarily as fat, protein, or carbohydrate) for later use, as
discussed below.
The hydrolysis of ATP to release energy is catalysed by a
number of different ATPase enzymes, each of which has a
specific function and a specific location in the cell. At rest, when
no contractile activity is taking place, the energy demand is
relatively low and most of the energy is used for the maintenance of electrical and ionic balances across the muscle membrane and across various internal membranes. The intracellular
concentration of potassium is high and the intracellular sodium
concentration is low; the concentrations are reversed outside the
c05.indd 54
cell. Maintaining these gradients requires energy. Biosynthetic
reactions such as protein synthesis and glycogen storage also
require an input of chemical energy.
In muscle, energy from the hydrolysis of ATP by myosin
ATPase activates specific sites on the force-developing elements, which try to increase the amount of overlap between the
actin and myosin filaments that make up the main structural
elements of the muscle. If the load on the muscle is less than
the force that can be generated, the muscle will shorten; if not,
force will be generated without any shortening, and so no external work will be done. Energy is still required whether or not
shortening of the muscle takes place. On activation of the
muscle, calcium is released into the cytoplasm from the storage
sites in the sarcoplasmic reticulum, and this calcium must be
removed in order for the muscle to relax and return to a resting
state. Active reuptake of calcium ions by the sarcoplasmic
reticulum requires ATP, as these ions must be pumped uphill
against a concentration gradient.
The mechanisms involved in the breakdown and resynthesis
of ATP can be divided into four main components:
1. ATP is broken down under the influence of a specific
ATPase to adenosine diphosphate (ADP) and inorganic
phosphate (Pi) in order to yield energy for muscle activity
or to power other reactions. This is the immediate source of
energy and all other energy-producing reactions must
channel their output through this mechanism.
2. Phosphocreatine (PCr) is broken down to creatine and phosphate; the phosphate group is not liberated as Pi, but is
transferred directly to an ADP molecule to re-form ATP.
This reaction is catalysed by the enzyme creatine kinase,
which is present in skeletal muscle at very high activities,
allowing the reaction to occur rapidly.
3. Glucose-6-phosphate, derived from muscle glycogen or
from glucose taken up from the bloodstream, is converted to
lactate and produces ATP by substrate-level phosphorylation reactions. These reactions do not require oxygen, and
so are commonly referred to as ‘anaerobic’.
4. The products of carbohydrate, lipid, protein, and alcohol
metabolism can enter the tricarboxylic acid (TCA) cycle
(also known as the Krebs cycle, after Sir Hans Krebs, who
first described it) in the mitochondria and be oxidized to
carbon dioxide and water. This process is known as oxidative phosphorylation and yields energy for the synthesis of
ATP.
The purpose of the last three mechanisms is to regenerate
ATP at sufficient rates to prevent a significant fall in the
intramuscular ATP concentration. If the ATP concentration
falls, the concentrations of ADP and adenosine monophosphate
(AMP) will rise. The concentration ratio of ATP to ADP and
AMP is a marker for the energy status of the cell. If the ratio
is high, the cell is in effect ‘fully charged’. This energy charge
is monitored in every cell: a fall in the ATP concentration or
a rise in the concentration of ADP or AMP will activate the
10/18/2010 5:11:21 PM
CHAPTER 1.5
metabolic pathways necessary to increase ATP production.
This is achieved by activation or inhibition of key regulatory
enzymes through changes in the concentration of the adenine
nucleotides.
The first three mechanisms identified above are all anaerobic
even when they occur in an environment where there is a plentiful supply of oxygen. Each uses only one specific substrate for
energy production (i.e. ATP, PCr and glucose-6-phosphate),
though the glucose-6-phosphate may be derived from either
glucose or glycogen. Glycerol, which is released into the circulation when triglycerides are broken down to make their component fatty acids available, can enter the glycolytic pathway
in liver and some other tissues. It does not appear to be an
energy source for skeletal muscle during exercise, probably
because of the lack of the enzyme glycerol kinase in muscle.
The aerobic (oxygen-using) processes in the mitochondria
metabolize a variety of substrates. The sarcoplasm contains a
variety of enzymes which can convert carbohydrates, lipids, and
the carbon skeletons of amino acids derived from proteins into
substrate, primarily a 2-carbon acetyl group linked to coenzyme
A (acetyl CoA); this can be completely oxidized in the mitochondria, resulting in production of ATP.
1.5.3.1
Phosphagen metabolism
If a muscle is poisoned with cyanide, which binds irreversibly
to the iron atoms in the enzyme cytochrome oxidase (as well
as to the iron atoms in haemoglobin and myoglobin, which
blocks oxygen transport), no energy can be provided by oxidative metabolism. If iodoacetic acid, which is an inhibitor of
glyceraldehyde 3-phosphate dehydrogenase (one of the enzymes
involved in the glycolytic pathway) and thus prevents ATP
formation by glycolysis, is also present, the muscle will still
appear to function normally for a short period of time before
fatigue occurs. This tells us that the muscle has another source
of energy which allows it to continue to generate force in this
situation; because fatigue occurs rapidly, this also tells us that
the capacity of this alternative energy source is limited. This
source is the intramuscular store of ATP and PCr (also known
as creatine phosphate); together these are referred to as the
phosphagens.
The most important property of the phosphagens is that the
energy store they represent is available to the muscle almost
immediately. With only a single reaction involved and an
enzyme with a very high activity, the PCr in muscle can be used
to resynthesise ATP at a very high rate. This high rate of energy
transfer corresponds to the ability to produce rapid forceful
actions by the muscles. The major disadvantage of this system
is its limited capacity: the total amount of energy available is
small. The major limitation again is the amount of creatine
phosphate that can be stored in the muscle: increasing stores
increases the osmolality inside the cells, which means that more
water moves into the muscles to maintain osmotic equilibrium.
The use of creatine supplements, however, does allow a relatively small increase in the amount of creatine phosphate stored
in the muscle, and this is associated with improvements in
c05.indd 55
BIOENERGETICS OF EXERCISE
55
strength and power. The use of creatine supplements is discussed in more detail elsewhere.
It may be important to note that the creatine kinase reaction
is actually slightly more complex than its usual representation.
Most textbooks show a simplified version of the equation as
follows:
PCr + ADP → ATP + Cr
At physiological pH and in the ionic environment of the cell
cytoplasm, however, PCr, ADP, and ATP are all dissociated to
some degree and carry a positive or negative charge, so a more
realistic representation of the reaction is:
PCr 2 + + ADP 3− + H + → ATP 4 − + Cr
From this, it is apparent that a hydrogen ion is consumed
when a phosphate group is transferred from PCr to ADP; that
is, the environment becomes more alkaline. This was actually
observed in early investigations of muscle metabolism, when
the muscle was stimulated to contract after being poisoned with
iodoacetic acid and cyanide as described above. This may be
more than just an interesting aside, as the muscle will normally
be generating large amounts of hydrogen ions as a result of the
breakdown of glycogen to lactate at the same time as the
demand for energy from the phosphagen store is at its peak.
These hydrogen ions result in acidification of the cytoplasm,
with negative consequences for some of the key enzymes of
glycolysis as well as for the control of actin and myosin interactions. Buffering some of these hydrogen ions by breaking down
PCr will allow more energy to be produced by glycolysis before
the pH in the muscle becomes dangerously low.
If no energy source other than the phosphagens is available
to the muscle, fatigue will occur rapidly. During short sprints
lasting only a few seconds (perhaps up to about 4–5), no
slowing down occurs over the last few metres – full power can
be maintained all the way – and the energy requirements are
met by breakdown of the phosphagen stores. Over longer distances, running speed begins to fall off, as these stores become
depleted and power output declines; the other energy sources
cannot regenerate ATP fast enough for maximum power to be
maintained. However, the rate of recovery from a short sprint
is quite rapid, and a second burst can be completed at the same
speed after only 2–3 minutes of recovery, provided that an
adequate supply of oxygen is available to allow for regeneration
of the PCr by production of ATP via oxidative metabolism. For
longer sprints, much longer recovery periods are needed before
the ability to produce a maximum performance is restored.
These observations tell us something about the rate of restoration of the pre-exercise chemical state of the muscle.
During sustained exercise, creatine and creatine phosphate
play a further important role in the cell, though this is often
neglected. Most of the ATP used by muscle cells is generated
by oxidative phosphorylation inside the mitochondria, but the
highest demand for ATP utilization during muscle contraction
occurs in the cytoplasm. The mitochondrial membrane is relatively impermeable to ATP and to ADP, so there must be an
10/18/2010 5:11:21 PM
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Myofibrils
Mitochondrion
ATP
ADP
Cr
PCr
Cr
ATP
PCr
ADP
Figure 1.5.1 In endurance exercise, most of the ATP hydrolysis
takes place in the cytoplasm of muscle cells but oxidative generation
of ATP takes place within the mitochondria. Because the
mitochondrial membrane is relatively impermeable to ATP,
translocation of energy equivalents is achieved by a creatinephosphocreatine shuttle.
alternative way of shuttling the energy produced by oxidative
metabolism to the sites where it is required. The primary
way in which this is achieved is by the transfer of ATP equivalents across the mitochondrial membrane in the form of PCr
(Figure 1.5.1).
1.5.3.2
The glycolytic system
Human skeletal muscle can exert force without the use of
oxygen as a consequence of its ability to generate energy anaerobically. Two separate systems are available to the muscle to
permit this; these are the phosphagen or high-energy phosphate
system described above and the glycolytic system. Because the
glycolytic system depends on the production of lactate while
the phosphagen system involves no lactate formation, they are
sometimes referred to as the lactic and the alactic systems,
respectively. The terms ‘lactic acid’ and ‘lactate’ are often used
interchangeably, but although lactic acid is perhaps a more
descriptive term, clearly indicating the acidic nature of the
molecule, lactate is more accurate and will be used here. At
physiological pH lactic acid is essentially entirely dissociated
to form lactate and hydrogen ions.
Under normal conditions, an isolated muscle incubated in
an organ bath and made to contract by application of an electrical stimulus clearly does not fatigue after only a few seconds
of effort, so a source of energy other than the phosphagens must
be available. This is derived from glycolysis, which is the name
given to the pathway involving the breakdown of glucose (or
glycogen). The end product of this series of chemical reactions,
which starts with a glucose molecule (C6H12O6) containing
six carbon atoms, is two 3-carbon molecules of pyruvate
(C3H3O3− or CH3COCOO−). This process does not use oxygen,
but does result in a small amount of energy in the form of ATP
c05.indd 56
Table 1.5.1 Capacity (the amount of work that can be done) and
power (the rate at which work can be done) of the energy supplying
metabolic processes available to human skeletal muscle. These values
are expressed per kg of muscle. They are approximations only and
will be greatly influenced by training status and other factors.
APT/CP Hydrolysis
Lactate formation
Oxidative metabolism
Capacity (J/kg)
Power (W/kg)
400
1000
800
325
200
being available to the muscle from reactions involving substratelevel phosphorylation. For the reactions to proceed, the pyruvate must be removed; when the rate at which energy is required
can be met aerobically, pyruvate is converted to carbon dioxide
and water by oxidative metabolism in the mitochondria. In
some situations the pyruvate is removed by conversion to
lactate, anaerobically, leading to the system being referred to
as the lactate anaerobic system.
Activation of the glycolytic system occurs almost instantaneously at the onset of exercise, despite the number of reactions
involved. All of the enzymes are present in the cytoplasm of
skeletal muscle at relatively high activities, and the primary
substrate (glycogen) is normally readily available at high
concentrations.
The total capacity of the glycolytic system for producing
energy in the form of ATP is large in comparison with the
phosphagen system (Table 1.5.1). In high-intensity exercise the
muscle glycogen stores are broken down rapidly, with a correspondingly high rate of lactate formation; some of the lactate
diffuses out of the muscle fibres where it is produced and
appears in the blood. A large part, but not all, of the muscle
glycogen store can be used for anaerobic energy production
during high-intensity exercise, and supplies the major part of
the energy requirement for maximum-intensity efforts lasting
from 20 seconds to 5 minutes. For shorter durations, the phosphagens are the major energy source, while oxidative metabolism becomes progressively more important as the duration (or
distance) increases.
Although the total capacity of the glycolytic system is
greater than that of the phosphagen system, the rate at which it
can produce energy (ATP) is lower (Table 1.5.1). The power
output that can be sustained by this system is therefore correspondingly lower, and it is for this reason that maximum speeds
cannot be sustained for more than a few seconds; once the
phosphagens are depleted, the intensity of exercise must necessarily fall.
The rate of lactate formation is dependant primarily on the
intensity of the exercise, but more on the relative exercise
intensity (%VO2max) than the absolute intensity. It is set by the
metabolic characteristics of the skeletal muscle and the recruitment patterns of the various muscle fibre types within the skeletal muscle.
The factors that integrate the metabolic response to exercise
so that energy supply can meet energy demand as closely as
possible are outlined below.
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CHAPTER 1.5
1.5.3.3 Aerobic metabolism: oxidation
of carbohydrate, lipid, and protein
Other pathways of regenerating ATP rely mainly on the provision of carbohydrate or lipid substrates from intramuscular
stores or from the circulation, and their subsequent breakdown
(catabolism) to yield energy through the reactions of the
electron transport chain and oxidative phosphorylation. To
regenerate ATP from lipid (fat) catabolism, oxygen is required,
as there is no mechanism that allows the energy content of the
fat molecules to be made available in the absence of oxygen.
This is in contrast to carbohydrate catabolism, which can occur
with or without the use of oxygen via the glycolytic pathway
described above.
The catabolism of glucose begins with anaerobic glycolysis,
which yields two molecules of pyruvate (or lactate) and two
molecules of ATP for each molecule of glucose that enters the
glycolytic pathway (although three molecules of ATP are
derived for each glucose moiety if the initial substrate is muscle
glycogen). In aerobic metabolism, mostly pyruvate (rather than
lactate) is formed and the 3-carbon pyruvate molecule is first
converted to a 2-carbon acetyl group which is bonded to an
activator group, coenzyme A (CoA), to form acetyl CoA. This
reaction is catalysed by the enzyme pyruvate dehydrogenase
(PDH). PDH is a complex enzyme that exists in both active and
inactive forms and is a key regulator in the integration of fat
and carbohydrate use through control of the rate of entry of
CHO fuel into the oxidative metabolic pathways. The catabolism of fatty acids also results in the formation of 2-carbon
acetyl units in the form of acetyl CoA. Acetyl CoA is the major
entry point for metabolic fuels into the TCA cycle.
In comparison to the catabolism of carbohydrate and lipid,
the breakdown of protein is usually a relatively minor source
of energy for exercise. Over the course of a day, the body
remains in protein balance, so the rate of breakdown and oxidation of the amino acids contained in protein must match the
amount of these amino acids present in the diet. Protein typically accounts for about 12–15% of total energy intake, so about
12–15% of energy must come from protein breakdown over the
day. In most situations, protein catabolism contributes less than
about 5% of the energy provision during physical activity.
Protein catabolism can provide both ketogenic and glycogenic
amino acids, which may eventually be oxidized either by deamination and conversion into one of the intermediate substrates
in the TCA cycle, or by conversion to pyruvate or acetoacetate
and eventual transformation to acetyl CoA. However, protein
catabolism can become an increasingly important source of
energy for exercise during starvation and in the later stages of
very prolonged exercise, when the availability of CHO is
limited.
1.5.4
THE TRICARBOXYLIC ACID
(TCA) CYCLE
The main function of the TCA cycle is to degrade the acetyl
CoA substrate to carbon dioxide and hydrogen atoms; the
c05.indd 57
BIOENERGETICS OF EXERCISE
57
metabolic machinery that allows this to take place is located
within the mitochondria. The hydrogen atoms are then oxidized
via the electron transport (respiratory) chain, allowing oxidative
phosphorylation and the subsequent regeneration of ATP from
ADP. The reactions of the TCA cycle will not be considered in
detail here and the interested reader is referred elsewhere (e.g.
Maughan and Gleeson, 2010).
The TCA cycle begins with the 2-carbon acetyl CoA, which
reacts with a 4-carbon molecule of oxaloacetate to form citrate.
Citrate then undergoes a series of reactions, during which it
loses two of these carbon atoms as CO2, resulting in regeneration of oxaloacetate, which is then free to react with another
acetyl CoA molecule and begin the cycle all over again. Some
of the energy released in these reactions is captured as ATP,
and one ATP molecule is formed during each turn of the cycle.
More of the available energy is captured by adenine nucleotides
(FAD and NAD). The overall reaction involving each molecule
of acetyl CoA is as follows:
acetyl CoA + ADP + 3NAD + + FAD → 2CO 2 + ATP + 3NADH
+ 3H + + FADH 2
Note that oxygen itself does not participate directly in the
reactions of the TCA cycle. In essence, the most important
function of the TCA cycle is to generate hydrogen atoms for
their subsequent passage to the electron transport chain by
means of NAD+ and FAD. The aerobic process of electron
transport–oxidative phosphorylation regenerates ATP from
ADP, thus conserving some of the chemical energy contained
within the original substrates in the form of high-energy
phosphates. As long as there is an adequate supply of O2, and
substrate is available, NAD+ and FAD are continuously regenerated and TCA metabolism proceeds.
The electron transport chain is a series of linked carrier
molecules which remove electrons from hydrogen and eventually pass them to oxygen; oxygen also accepts hydrogen to form
water. Much of the energy generated in the transfer of electrons
from hydrogen to oxygen is trapped or conserved as chemical
potential energy in the form of high-energy phosphates, the
remainder is lost as heat.
In terms of the energy conservation of glucose metabolism,
the overall reaction starting with glucose as the fuel can be
summarized as follows:
glucose + 6 O 2 + 38 ADP + 38 Pi → 6 CO 2 + 38 ATP
The corresponding equation for oxidation of a typical fatty
acid can be expressed as:
palmitate + 23 O2 + 130 ADP + 130 Pi → 6 CO 2 + 146 H 2 O
+ 130 ATP
It may seem from this that fat is the best fuel to use, especially as it is present in almost unlimited amounts, in contrast
to the small body stores of carbohydrate, but there are several
considerations to bear in mind. First, carbohydrate is a much
more versatile fuel, as it can be used to generate energy in the
absence of oxygen. Second, the maximum rate of oxidative
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energy supply using carbohydrate as a fuel is typically about
twice as high as that achieved when fat is used. Third, carbohydrate is a more ‘efficient’ fuel in that the oxygen cost is less
than that when fat is used. Even though this difference is relatively small (about 5.01 kcal/l for CHO as opposed to about
4.7 kcal/l for fat), it may be crucial when the oxygen supply is
limited. A greater oxygen demand by the working muscles
means that they need a greater blood flow, and this may result
in diversion of blood away from other tissues.
1.5.5
OXYGEN DELIVERY
As the rate of energy demand increases in exercise, so the
rate of oxygen consumption also increases, at least up until a
finite point is reached beyond which there is no further increase.
At low- to moderate-intensity exercise, there is a good linear
relationship between power output and oxygen consumption.
At high-power outputs, however, the curve becomes exponential. In well-motivated and reasonably fit individuals, a point
is reached at which there is no further increase in oxygen
consumption even when the power output is increased. This
point was defined by Hill and Lupton in 1923 as the individual’s maximum oxygen uptake (VO2max). Clearly, the energy
demand continues to increase as the power output is increased,
and the shortfall in energy provision is met by anaerobic
metabolism. Where no plateau is reached, the highest oxygen
uptake achieved is referred to as the peak oxygen uptake
(VO2peak).
There has been, and remains, much debate as to what limits
the maximum oxygen uptake. In some experimental models, it
may be limited by the ability of the lungs to oxygenate the
arterial blood, by the ability of the muscles to use oxygen, or
perhaps by other factors. The evidence, however, is overwhelmingly in support of the limitation lying in the ability of the heart
to supply blood to the working muscles (Ekblom and Hermansen,
1968). Forty years of further research and much debate have
not altered this viewpoint (Levine, 2008).
There is some inertia in the oxygen transport/oxygen utilization system, and whereas the demand for energy increases more
or less immediately at the start of exercise, it takes some time
for oxygen uptake to reach its peak level. The kinetics of
oxygen uptake at the onset of exercise has been investigated
extensively and it is clear that many factors will influence this
response (Jones and Poole, 2005). In moderate exercise at constant power output there is a rapid increase in the rate of oxygen
consumption at the onset of exercise, with a relatively steady
state being achieved after about 2–3 minutes. Over time,
however, there will be a slight upward drift in the oxygen consumption, accompanied by an upward drift in heart rate and
other physiological parameters. Many factors contribute to this,
including a progressive increase in the contribution of fat oxidation to oxidative energy supply relative to the contribution of
CHO. For each litre of oxygen used, CHO oxidation will
provide 5.01 kcal (21.0 kJ) of energy, while fat oxidation provides about 4.69 kcal (19.6 kJ), which is about 6% less (Jéquier
et al., 1987).
c05.indd 58
The shortfall in energy supply in the first few minutes of
exercise is met by anaerobic metabolism, as outlined above.
Without this, the rate of acceleration at the onset of exercise
would be set by the rate of oxidative metabolism. Rapid acceleration would be impossible, and full speed would not be
reached until after 2–3 minutes. In evolutionary terms this
would not be a good survival strategy. Humans are well
equipped for both rapid accelerations (relying on anaerobic
metabolism) and sustained exercise (relying on aerobic metabolism). Both of these assets are important where success in
escape from predators and the pursuit of prey will determine
survival of the individual and of the species.
One of the key adaptations to endurance training is an
increase in the capacity for energy supply by oxidative metabolism, and a high VO2max has long been recognized as one of the
distinguishing characteristics of the elite endurance athlete.
This is accompanied by changes in the cardio-respiratory
system and within the trained muscles themselves. Crosssectional comparisons of individuals of differing training status,
and longitudinal studies of the adaptations to a short-term
endurance programme, both show that:
Endurance training is accompanied by an increased maximum
cardiac output.
Endurance
training is accompanied by increases in the
capacity of the muscles to generate energy by oxidative
metabolism.
Both of these adaptations tend to occur in parallel, accounting at least in part for the debate as to whether oxygen supply
or oxygen use is the limitation to VO2max.
1.5.6 ENERGY STORES
Energy intake comes from the food we eat, specifically from
the energy-containing macronutrients, carbohydrate, fat,
protein, and alcohol. Alcohol cannot be stored and must be
metabolized immediately, but the other fuels can either be used
immediately as energy sources or stored for later use. Protein
is not stored, in the sense that all proteins are functionally
important molecules (e.g. structural proteins, enzymes, ion
channels, receptors, contractile proteins, etc.), and the concentration of most free amino acids in intracellular and extracellular body fluids is too low for these to be of any significance.
Loss of structural and functional proteins inevitably involves
some loss of functional capacity, but this may be tolerable when
no alternative energy source is available, as in periods of prolonged starvation. Though it is usually accepted that there is no
protein store in the human body, it must be remembered that
the rate of protein turnover in gut tissues is extremely high: gut
mucosal protein synthesis occurs over 30 times faster than that
of skeletal muscle (Charlton, Ahlman and Nair, 2000). In the
early stages of fasting, there will be some loss in intestinal
tissue mass, making the amino acids released from breakdown
of gut tissue available for protein synthesis in other tissues. This
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CHAPTER 1.5
probably occurs after only a few hours without food, and it may
therefore be viewed as a store of protein.
Carbohydrates are stored in the body in only very limited
and rather variable amounts. The size of the carbohydrate stores
is very much influenced by the diet and exercise activity in the
preceding hours and days. The availability of endogenous carbohydrate is not a problem for the organism when regular intake
of carbohydrate foods is possible, or when the demand for
carbohydrate is low, but regular hard exercise can pose a major
challenge. Glycogen is the storage form of carbohydrate in
animals, analogous to the storage of starch in plants. The glycogen molecule is a branched polymer consisting of many (typically 50 000–100 000) molecules of glucose joined together by
α1,4-bonds; branch points are introduced into the chains of
glucose molecules when an additional α1,6-bond is formed.
The advantage of these polymers is that relatively large amounts
of carbohydrate can be stored without the dramatic increase in
osmolality that would occur if the same amount of carbohydrate
were present as glucose monomers.
Skeletal muscle contains a significant store of glycogen,
which can be seen under the electron microscope as small
granules in the sarcoplasm. The glycogen content of skeletal
muscle at rest in well-fed humans is approximately 14–18 g per
kg wet mass (about 80–100 mmol glucosyl units/kg). The liver
also contains glycogen; about 80–120 g is stored in the liver of
an adult human in the post-absorptive state, which can be
released into the circulation in order to maintain the blood
glucose concentration at about 5 mM (0.9 g per litre). The liver
glycogen store falls rapidly during fasting and during prolonged
exercise, as glucose is released into the circulation to maintain
the blood glucose concentration (Hultman and Greenhaff,
2000). Considering that glucose can be oxidized at rates of
2–4 g/min during prolonged exercise, it is apparent that the
blood glucose cannot be considered as any form of carbohydrate ‘store’ but is rather only the transit form that allows
glucose to be moved between tissues.
Early studies of fuel use during exercise relied on measures
of oxygen uptake and the respiratory exchange ratio. While
these allowed determination of the rates of fat and CHO oxidation, they did not enable the sources of these fuels to be
determined. Application of the muscle biopsy technique to the
study of human metabolism began in Scandinavia the early1960s. In a classic study (Bergstrom and Hultman, 1966),
a one-legged cycling model was used to show that prolonged
exercise resulted in depletion of the glycogen store in the
exercise muscle but not in the resting muscle. Although there
were only two subjects (the authors themselves), they were
also able to show that subsequent re-feeding of a highcarbohydrate diet for three days resulted in abnormally high
levels of glycogen storage in the exercise muscles but had no
effect on the resting muscles. Soon afterwards, it was shown
that exercise capacity was closely related to the size of the
pre-exercise muscle glycogen store (Ahlborg et al., 1967;
Bergstrom et al., 1967). These observations and others published at around the same time were to set the tone for much
of the sports nutrition advice given to athletes up until the
present day. More recently, other methodologies have helped
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BIOENERGETICS OF EXERCISE
59
to elucidate the contribution of fuels to energy metabolism:
these include isotopic tracer methods and, more recently, the
use of non-invasive methods such as magnetic resonance
spectroscopy.
The major storage form of energy in the human body is lipid,
which is stored as triglyceride (triacylglycerol), mainly in
adipose tissue. The total storage capacity for lipid is extremely
large, and for most practical purposes the amount of energy
stored in the form of fat is far in excess of that required for any
exercise task (Table 1.5.2). Even in the leanest individual, at
least 2–3 kg of triglyceride is stored. Such low levels would
seldom be encountered in healthy individuals, but they are not
uncommon in elite male marathon runners (Pollock et al.,
1977). Women generally store much more fat than men, but
elite female athletes also have a very low body fat content
(Wilmore, Brown and Davis, 1977). It is not unusual to see
triglyceride accounting for 30–40% of total body mass in sedentary individuals. These adipose tissue depots are located
mainly under the skin (subcutaneous depots) or within the
abdominal cavity.
Triglyceride mobilized from the adipose tissue stores must
first be broken down by a lipase enzyme to release free fatty
acids (FFAs) into the circulation for uptake by working muscle.
Skeletal muscle also contains some triacylglycerol stored
within the muscle cells, as well as some adipose cells within
the muscle. The intramuscular triglyceride (IMTG) is present
as small lipid droplets within the cell and many of these are in
close proximity to the mitochondria, where they will be oxidized when required. These IMTG stores can account for about
20% of total energy supply, or about 30–50% of the total
amount of fat oxidized during prolonged moderate-intensity
exercise (Stellingwerff et al., 2007). This source of fuel may
become relatively more important after exercise training, when
the capacity for fat oxidation is greatly increased. Study of the
role of the triglyceride stored within the muscle cells has been
hindered by the difficulties in making accurate measurements
of these relatively small stores of fat, but their significance is
now being appreciated. This is in part due to improved methods
for measuring IMTG; these methods include measures on
muscle biopsy samples (biochemical analysis, electron microscopy, and histochemistry), as well as newer, non-invasive
alternatives (computed tomography, magnetic resonance spectroscopy, magnetic resonance imaging). The contribution of
Table 1.5.2 Energy stores in a typical 70 kg man in a fed and rested
state. These can vary greatly between individuals and can also vary
substantially over time within an individual.
Carbohydrate stores
Blood glucose
Liver glycogen
Muscle glycogen
Fat stores
Adipose tissue
Muscle triglyceride
3–5 g
80–100 g
300–400 g
3–20 kg
500 g
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intramuscular lipid to total energy turnover during a period of
prolonged exercise will be influenced by many factors, including training status, pre-exercise diet, and gender (Roepstorff,
Vistisen and Kiens, 2005). While the adipose triglyceride may
amount to 10–50% of body mass, the intramuscular store is
much smaller, at about 300 g. The IMTG content of highly
oxidative muscle fibres is much higher than that of the fasttwitch, glycolytic fibres (Schrauwen-Hinderling et al., 2006).
As with muscle glycogen stores, the IMTG store is influenced
by diet and can be increased by eating a high-fat diet (Zehnder
et al., 2006). This in turn leads to an increased reliance on this
fuel source during exercise. Increased levels of intramuscular
fat are associated with obesity, diabetes, and insulin resistance,
but stores are also higher in well-trained endurance athletes,
who normally have low levels of adipose tissue triglyceride
(Tarnopolsky et al., 2006).
Lipid stores in the body are far larger than those of carbohydrate, and lipid is a more efficient storage form of energy,
releasing 37 kJ for each gram oxidized, compared with 16 kJ/g
for carbohydrate. Each gram of carbohydrate stored also retains
about 1–3 g of water, further decreasing the efficiency of carbohydrate as an energy source. The energy cost of running a
marathon for a 70 kg runner is about 12 000 kJ; if this could
be achieved by the oxidation of fat alone, the total amount
of lipid required would be about 320 g, whereas 750 g of carbohydrate would be required if carbohydrate oxidation were
the sole source of energy. Apart from considerations of the
weight to be carried, this amount of carbohydrate exceeds the
total amount normally stored in the liver and the muscles
combined. By comparison, we can calculate the amount of
ATP required to run a marathon if the only energy source
available to the muscle were ATP. The energy cost of running
can be expressed as the oxygen demand, which is equivalent
to about 600 l of oxygen consumption for the 70 kg runner
quoted above.
For simplicity, we might assume that all the energy comes
from oxidation of carbohydrate. The equation for ATP generation from glucose oxidation is:
C6 H12 O6 + 6 O 2 → 6 CO 2 + 6 H 2 O + 36 ATP
c05.indd 60
Substituting the molecular weight of the reactants, we get:
180 g glucose + 192 g O2 → 264 g CO 2 + 108 g H 2 O
+ 18.25 kg ATP
One mole of a gas occupies 22.4 l at standard temperature
and pressure, so we can recalculate this equation as:
180 g glucose + 134.4 l O 2 → 134.4 l CO 2 + 108 g H 2 O
+ 18.25 kg ATP
From this, we can calculate that 0.136 kg of ATP is resynthesized for each litre of O2 consumed. Because 600 l of O2 was
used for the marathon, this means that the total mass of ATP
required to complete the distance was 82 kg, more than the runner ’s total body mass. Compared to this, the amounts of fat and
carbohydrate consumed are rather small. It is not surprising then
that in most situations carbohydrate and lipids supply most of
the energy required to regenerate the ATP needed to fuel
exercise.
1.5.7
CONCLUSION
The rate of energy provision to cells must equal the rate of
energy consumption to prevent potentially damaging disturbances to cell homeostasis. Muscle cells are uniquely equipped
to cope with sudden changes in the rate of energy supply and
with high rates of energy supply. Cells use the energy released
by the hydrolysis of the terminal phosphate bond of the ATP
molecule, but the cellular ATPO content cannot fall much
below the resting level without irreversible cell damage. Three
main mechanisms contribute to ensuring that ATP is resynthesised as fast as it is hydrolysed. These are: 1. the transfer of a
phosphate group from creatine phosphate; 2. substrate level
phosphorylation involving degradation of glycogen or glucose
to pyruvate; 3. oxidative phosphoyrlation. Various combinations of these three metabolic pathways allow for the very high
energy demands of a 100 m spring and for the sustained demands
of a marathon run. From a biochemical perspective, fatigue is
simply an inability to meet the body’s energy demand.
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CHAPTER 1.5
References
Ahlborg B., Bergstrom J., Ekelund L.-G. and Hultman E.
(1967) Muscle glycogen and muscle electrolytes during
prolonged physical exercise. Acta Physiol Scand, 70,
129–142.
Bergstrom J. and Hultman E. (1966) Muscle glycogen
synthesis after exercise: an enhancing factor localized to
the muscle cells in man. Nature, 210, 309–310.
Bergstrom J., Hermansen L., Hultman E. and Saltin B. (1967)
Diet, muscle glycogen and physical performance. Acta
Physiol Scand, 71, 140–150.
Charlton M., Ahlman B. and Nair K.S. (2000) The effect of
insulin on human small intestinal mucosal protein
synthesis. Gastroenterology, 118, 299–306.
Ekblom B. and Hermansen L. (1968) Cardiac output in
athletes. J Appl Physiol, 25, 619–625.
Hill A.V. and Lupton H. (1923) Muscular exercise, lactic
acid, and the supply and utilization of oxygen. Q J Med,
16, 135–171.
Hultman E. and Greenhaff P.L. (2000) Carbohydrate
metabolism in exercise, in Nutrition in Sport (ed. R.J.
Maughan), Blackwell, Oxford, pp. 85–96.
Jéquier E., Acheson K. and Schutz Y. (1987) Assessment of
energy expenditure and fuel utilization in man. Ann Rev
Nutr, 7, 187–208.
Jones A.M. and Poole D.C. (2005) Oxygen Uptake Kinetics in
Sport, Exercise and Medicine, Routledge, London.
Levine B.D. (2008) VO2max: what do we know and what do
we still need to know? J Physiol, 586, 25–34.
Maughan R.J. and Gleeson M. (2010) The Biochemical Basis
of Sports Performance, 2nd edn. Oxford University Press,
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Pollock M.L., Gettman L.R., Jackson A. et al. (1977)
Body composition of elite class distance runners.
Ann NY Acad Sci, 301, 361–370.
Roepstorff C., Vistisen B. and Kiens B. (2005)
Intramuscular triacylglycerol in energy metabolism
during exercise in humans. Exerc Sport Sci Rev, 33,
182–188.
Schrauwen-Hinderling V.B., Hesselink M.K.,
Schrauwen P. and Kooi M.E. (2006) Intramyocellular
lipid content in human skeletal muscle. Obesity, 14,
357–367.
Stellingwerff T., Boon H., Jonkers R.A. et al. (2007)
Significant intramyocellular lipid use during prolonged
cycling in endurance-trained males as assessed by three
different methodologies. Am J Physiol Endocrinol
Metab, 292, E1715–E1723.
Tarnopolsky M.A., Rennie C.D., Robertshaw H.A. et al.
(2006) Influence of endurance exercise training and
sex on intramyocellular lipid and mitochondrial
ultrastructure, substrate use, and mitochondrial enzyme
activity. Am J Physiol Regul Integr Comp Physiol,
292, R1271–R1278.
Wilmore J.H., Brown C.H. and Davis J.A. (1977) Body
physique and composition of the female distance runner.
Ann NY Acad Sci, 301, 764–776.
Winter E.M. and Fowler N. (2009) Exercise defined and
quantified according to the Systeme International d’Unites.
J Sports Sci, 27, 447–460.
Zehnder M., Christ E.R., Ith M. et al. (2006) Intramyocellular
lipid stores increase markedly in athletes after 1.5 days
lipid supplementation and are utilized during exercise in
proportion to their content. Eur J Appl Physiol, 98,
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1.6 Respiratory and Cardiovascular
Physiology
Jeremiah J. Peiffer1 and Chris R. Abbiss2,3,4, 1 Murdoch University, School of Chiropractic and Sports Science,
Murdoch, WA, Australia, 2 Edith Cowan University, School of Exercise, Biomedical and Health Sciences,
Joondalup, WA, Australia, 3 Australian Institute of Sport, Department of Physiology, Belconnen, ACT, Australia,
4
Commonwealth Scientific and Industrial Research Organisation, Division of Materials Science and Engineering,
Belmont, VIC, Australia
1.6.1
1.6.1.1
THE RESPIRATORY SYSTEM
Introduction
Often overlooked, the respiratory system is an important component in overall health as well as in athletic performance.
Its key role is to facilitate the exchange of oxygen (O2) from
the ambient air into the blood stream, in addition to removing
metabolic carbon dioxide (CO2) from the body. The respiratory system may appear simplistic, but in actuality respiratory
function is complex, involving a combination of mechanical
actions directed by neural drive. The following pages present
a basic overview of this system. After reading this section
you should be able to explain: (1) the basic anatomy of the
respiratory system, (2) gas exchange in the lungs and the role
of diffusion, (3) how ventilation occurs at rest and during
exercise, and (4) the mechanical and neural controls of
ventilation.
1.6.1.2
Anatomy
The respiratory system comprises two sections, the conducting
zone and the respiratory zone (Figure 1.6.1). During ventilation,
ambient air will enter the nose or mouth and travel through the
conducting zone, passing first through the trachea and then
proceeding into the primary bronchus. From the primary bronchus, air will descend into the left and right bronchi and further
into the smaller, yet more abundant, bronchioles. The conducting zone provides an area for air filtration, humidification, and
warming; nonetheless, no gas exchange occurs there, and thus
it is commonly referred to as dead space.
After travelling through the conducting zone, ventilated air
will proceed into the respiratory zone. From the bronchioles,
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
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the oxygen-rich air passes through the respiratory bronchioles,
into the alveolar ducts, and finally into the alveolar sac.
Thousands of alveoli, positioned like grapes on a grape vine,
make up each alveolar sac, and it is possible for the lungs to
contain more than 600+ million individual alveoli. A thin membranous tissue surrounds each alveoli, which when filled with
air will stretch, further reducing the alveoli wall thickness (like
a balloon being filled with air). Helping alveolar expansion, the
internal walls of each alveoli are covered in a substance called
surfactant which acts to decrease surface tension. On the outer
surface of the alveoli is a complex network of capillaries. Due
to the thickness of the alveolar membrane, and the close proximity to the capillaries, the alveoli are the primary point of gas
exchange in the lung.
1.6.1.3
Gas exchange
The exchange of O2 and CO2 between the lungs and the blood
is essential to human life. As highlighted in the previous section,
alveolar structure and the close proximity of the surrounding
capillaries provide an optimal environment for gas exchange.
The movement of O2 and CO2 between the alveoli and blood
occurs through the diffusion of these molecules through the
alveolar wall, across the interstitial fluid, and through the capillary wall (Figure 1.6.2). The control of diffusion is determined
by a combination of factors, including: (1) diffusion distance,
(2) surface area, and (3) pressure gradients.
Diffusion distance and surface area
The thickness of the alveolar wall (approximately 0.1 micron)
and the small volume of interstitial fluid between the alveoli
and the capillaries result in very low resistance for the diffusion
of O2 and CO2 (McArdle, Katch and Katch, 2004). Additionally,
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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Figure 1.6.1 The anatomy of the human respiratory system
the sheer number of alveoli (600+ million) comprising the
alveolar sacs provides a massive surface area on which gas
exchange can occur; if all the alveoli in the lung were removed
from the body and laid flat on the ground, their surface area
would be great enough to cover half a standard tennis court. It
is important to note, however, that disease can affect the diffusion distance and/or the surface area available for diffusion,
resulting in a decrease in gas exchange (Comroe et al., 1964).
Pressure gradients
The rate of diffusion for O2 and CO2 is influenced by the pressure gradients for each in the lungs and the blood. When the
pressure gradient between the alveoli and the blood is high, O2
will rapidly cross the alveolar membrane (Figure 1.6.2a).
Nevertheless, this process is not without end. Diffusion is governed by Henry’s law, which states that the diffusion of a
molecule across a membrane is influenced by not only the pressure difference between the two mediums but also the ability
of the molecule to dissolve in the accepting medium. The movement of O2 and CO2 from areas of high to low pressure will
alter the original pressure of each medium (Figure 1.6.2b),
lowering the pressure gradient and decreasing the movement of
molecules. At a terminal point, the partial pressures between
c06.indd 64
the two areas will be in equilibrium (at similar pressures) and
the movement of molecules will cease (Figure 1.6.2c).
In the human body, the pressure gradients that control the
movement of O2 are a product of the environment. For instance,
ambient air primarily comprises three types of gas: nitrogen
(N2), oxygen (O2), and carbon dioxide (CO2). As a percentage,
N2 makes up the majority (79%), followed by O2 (21%), and
then CO2 (0.03%). At sea level, the atmospheric pressure of
air is approximately 760 mmHg. When combined with the
percentage composition of air, the partial pressure of each gas
can be calculated. For example, the partial pressure of O2 (PO2)
at sea level is: 760 mmHg × 0.2095 = 160 mmHg. Using the
same technique, PCO2 (0.2 mmHg) and PN2 (600 mmHg) can be
calculated.
While the ambient air PO2 can easily be calculated as in the
previous example, upon entering the body the PO2 is immediately reduced. In the conducting zone of the respiratory system,
ambient air becomes 100% saturated with water vapour. In the
presence of water vapour, all other partial gas pressures are
diluted, and therefore the total pressure of the air entering the
body is reduced by the PH2O (47 mmHg) at body temperature
(37 °C). Thus, ambient air entering the respiratory zone has a
PO2 of 150 mmHg, or 10 mmHg lower than in sea-level ambient
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CHAPTER 1.6
RESPIRATORY AND CARDIOVASCULAR PHYSIOLOGY
65
Figure 1.6.2 Schematic of gas exchange between the alveoli and venous blood. As alveolar pressure is high (a), O2 is transported rapidly from
the alveoli to the blood. However, as O2 dissolves in the blood the pressure gradients begin to equilibrate (b), until the pressure gradient is in
equilibrium (c). Circles = alveoli and boxes = capillaries
Figure 1.6.3 Schematic representation of the transport of O2 and CO2 between the alveoli and blood. Pa = partial pressure in the arteries,
Pv = partial pressures in the vein, PA = partial pressure in the alveoli
air. At the alveoli (primary site of diffusion), PO2 will again
have been reduced due to some diffusion of O2 outside the
alveoli and the increase in diffused CO2 from the blood. Indeed,
at the time of diffusion in the alveoli, the final alveolar partial
pressure (PA) of O2 is approximately 105 mmHg, or 55 mmHg
c06.indd 65
less than in sea-level ambient air (Brooks et al., 2000; West,
1962).
Even with a 55 mmHg loss in pressure, the pressure gradient
for O2 is still large enough to facilitate the transport of O2 from
the alveoli to the blood (West, 1962). As shown in Figure 1.6.3,
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blood returning from the systemic circulation has a venous PO2
of 40 mmHg and a PCO2 of 46 mmHg; therefore, the pressures
in the alveoli (PAO2 = 100 mmHg and PACO2 = 40 mmHg) create
a diffusion gradient of 60 mmHg for O2 and 6 mmHg for CO2.
Surprisingly, while the diffusion gradient for CO2 is much
lower than that for O2, CO2 is still rapidly transported across
the alveolar membrane due to a greater diffusion capacity for
CO2 compared with O2 (approximately 20x greater) (Brooks
et al., 2000). Upon exiting the lung, the arterial pressures
of O2 (PaO2) and CO2 (PaCO2) are 100 mmHg and 40 mmHg,
respectively.
1.6.1.4
Mechanics of ventilation
Negative pressure
Similar to the exchange of O2 and CO2 within the alveoli,
the mechanisms behind ventilation are influenced by changes
in pressure gradients. As shown in Figure 1.6.1, both the left
and right lobes of the lungs are connected, at their distal
ends, to the diaphragm muscle. During inhalation, the contraction of the diaphragm results in a lengthening of the lung
(pulling downward), which creates a negative pressure.
Opening the mouth during this time facilitates the flow of
higher-pressure room air into the respiratory system. Imagine
you have covered the top of a syringe with your finger;
pulling down on the plunger creates suction by increasing
the volume in the chamber and creating negative pressure,
much like the diaphragm and lung. During expiration, the
diaphragm relaxes and the small muscles between the ribs
(the intercostal muscles) contract around the lung, causing an
increase in lung pressure and the expelling of air. Contraction
and relaxation of the diaphragm and intercostals can be
controlled by both conscious and subconscious means (discussed in later sections).
Static lung volumes
The size of an individual’s lung is influenced predominately by
genetic factors. Although it has been suggested that endurance
training can increase lung size, this statement is completely
false. Instead, total lung volume is primarily a function of an
individual’s gender, age, and most importantly height (Cotes
et al., 1979). The normal range for total lung volume in males
and females is between 3.0 and 6.0 L, with the greatest volumes
observed in taller men.
Figure 1.6.4 is a fictional tracing of the static lung volumes
in the human body. The word ‘static’ suggests that these
volumes do not normally change, but certain pulmonary disorders can reduce lung volumes, and recently specific respiratory muscle training has been shown to increase some volumes.
During normal ventilation, we breathe in a rhythmic fashion;
the air that is ventilated in and out of the lung is known as
tidal volume (TV). The additional volumes above and below
the TV represents the additional capacity for ventilation and
are known as the inspiratory reserve volume (IRV) and the
expiratory reserve volume (ERV). Together, the IRV, ERV,
and TV make up the forced vital capacity (FVC). You should
notice that a small volume of air remains below the FVC. This
space is known as the residual volume (RV) and is a nonventilating volume of air; it is essential as it helps to maintain
lung structural integrity. The total lung capacity (TLC) therefore comprises both ventilating (FVC) and nonventilating (RV)
areas of the lung.
During rest, only a small portion of the FVC is used by the
TV. As exercise begins, the frequency of breathing increases
(the respiratory rate, RR), as does the volume of air ventilated
Figure 1.6.4 Diagram of lung volumes measured from helium dilution spirometery
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RESPIRATORY AND CARDIOVASCULAR PHYSIOLOGY
per breath. Together, these increase the minute ventilation (VE)
(explained in detail later). The increase in TV encroaches into
both the IRV and the ERV. Nevertheless, more IRV is utilized
during the increase in TV than ERV. It should be noted,
however, that even during intense exercise TV rarely exceeds
60% of the IRV (Guenette et al., 2007).
Dynamic lung volumes
During a given exercise bout, static lung volumes do not
change. For this reason, increasing pulmonary ventilation to
meet the demands of exercise requires rapidly increasing the
rate of ventilation. For example, during maximal exercise in
highly trained individuals, VE can increase to approximately
37 times the resting rate (rest = 6 l/min; maximal = 220 l/min).
Such high ventilatory rates are achievable due to changes in
dynamic lung volumes. Compared to static volumes, dynamic
lung volumes have a greater capacity to change with training
status (Doherty and Dimitriou, 1997). Measuring dynamic lung
volume can indicate an individual’s capacity to reach high
ventilatory rates during exercise; common measurements
include forced expiratory volume over one second (FEV1) and
maximal voluntary ventilation (MVV). During measures of
FEV1, individuals are instructed to inhale maximally and then
exhale as fast and forcefully as they can for six seconds. The
FEV1 is the volume of air expired during the first second of
expiration. This value is compared with the FVC; in normal
healthy individuals the FEV1 : FVC ratio should be greater than
80% (Figure 1.6.5). Ratios recorded below this value may be
indicative of pulmonary obstructive disease (Comroe et al.,
1964). The measurement of MVV can indicate an individual’s
maximal ability to ventilate. During this test, individuals are
67
required to breathe as deeply and rapidly as possible for 15
seconds. The total amount of ventilation (in L) is then extrapolated to represent a one-minute value (l/min), which is compared to age- and gender-normative values. In individuals with
pulmonary disorders MVV is usually less than 50% of the age
and gender norms (Kenney et al., 1995).
As previously stated, with the appropriate training both
static and dynamic lung volumes can be altered. With the use
of specifically designed respiratory training devices, respiratory
muscle training can increase both FEV1 and FVC (Wells et al.,
2005). In addition, respiratory muscle training has been shown
to increase the force of inspired and expired ventilation, and
MVV (Wells et al., 2005). Further, respiratory muscle training
can increase endurance performance and recovery from highintensity exercise (Romer, McConnell and Jones, 2002a,
2002b). While the increase in performance is not directly linked
to changes in lung volumes, other proposed mechanisms have
been suggested for the change in performance, including:
decreases in respiratory blood flow, decreases in perceived
exertion, and lower respiratory muscle fatigue.
1.6.1.5 Minute ventilation
At rest, there is little demand on the pulmonary system to
increase the availability of O2 and the removal of CO2. For this
reason, in a resting state pulmonary VE is quite low (∼6 l/min);
it is a product of a low TV (∼0.5 L per breath) and RR (12
breaths per minute) (Table 1.6.1). During exercise, there is an
increase in the demand for O2 and in the need to remove accumulated CO2. For this reason, VE is increased by increasing both
Figure 1.6.5 Theoretical tracing from a pulmonary function test
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Table 1.6.1 Typical VE and TV measurements in a male at rest and
during moderate and maximal cycling exercise
VE (l/min)
TV (l/breath)
RR (breaths/minute)
Resting
Moderate
exercise
Maximal
exercise
6
0.5
12
77
2.6
28
207
5.0
41
the TV and the RR. Although VE can be increased by increases
in either of these values alone, the ability to obtained high
minute ventilatory rates, as seen during maximal exercise,
requires a combination of both.
1.6.1.6
Control of ventilation
Ventilatory control is achieved on both a conscious and an
subconscious level. In most circumstances, breathing is controlled primarily by subconscious mechanisms, mediated by
complex feedback signals from chemical receptors located in
the periphery and brain, as well as by mechanical receptors
in the lungs, both of which continuously send signals to the
respiratory centre of the brain (medulla), otherwise known as
the central controller (for review see Corne and Bshouty, 2005).
However, humans are capable of overriding normal subconscious control of their ventilation; during instances of prolonged
holding of breath or purposeful hyperventilation, humans can
consciously override central and peripheral feedback signalling.
Nevertheless, at some point the subconscious drive will overcome the conscious drive and control of ventilation will once
again return to a level of homoeostasis.
Chemical receptors
Ventilatory chemical receptors are located both in the periphery
and centrally within the brain. The primary function of chemical
receptors is to monitor the levels of PaO2, PaCO2, and blood pH.
In the periphery, chemical receptors are located in both the
aortic arch and the right and left carotid arteries. The close
proximity of the aortic and carotid chemical receptors to the left
ventricle allows for the rapid assessment of the blood being
pumped to the periphery. The response of peripheral receptors
to PaO2 is hyperbolic in nature; therefore, small changes in PaO2,
within normal ranges (>75 mmHg), have little effect on peripheral receptors and thus little influence on ventilation.
Nevertheless, if PaO2 falls below 75 mmHg the action of the
peripheral receptors is increased in an exponential manner. In
contrast to PaO2, chemical receptors have a significantly greater
sensitivity to PaCO2 and pH. At a normal PaO2 (100 mmHg), the
response to changes in PaCO2 is linear, indicating that small
changes in PaCO2 can have large effects on ventilation (i.e.
increasing PaCO2 = increasing ventilation). In addition, the production of metabolic CO2 is often accompanied by an increase
in H+ and thus a decrease in pH. Low pH levels are associated
with an increase in peripheral chemical receptor sensitivity
c06.indd 68
to PaCO2. Therefore, during exercise where metabolic CO2 production is high, the level of PaCO2 is a major driving force for
peripheral chemical receptor control of ventilation.
While the peripheral chemical receptors are responsive to
changes in blood PaO2, PaCO2, and pH, central chemical receptors
respond primarily to increases and decreases in PaCO2 and the
resultant changes in cerebral spinal fluid pH. Central chemical
receptors are located in the medulla and several places in the
brain stem. Due to their heightened sensitivity to PaCO2 and pH,
the effect of central chemical receptors on ventilation is large.
Indeed, central chemical receptors account for over 70% of the
chemical receptor control of ventilation.
Mechanical receptors
Although a large majority of ventilatory control is dictated by
central and peripheral chemical receptors, additional mechanical receptors found in the lungs can also mediate respiratory
action. Within the lung, two receptors have been observed
which produce afferent feedback to the central controller.
Located within the smooth muscle of the lung are peripheral
stretch receptors, myelinated receptors sensitive to changes in
lung volumes. In circumstances where lung volumes are high
(e.g. exercise), the peripheral stretch receptors send signals to
the central controller resulting in a shortened inspiration and a
lengthened expiration. Conversely, located in the upper airways
are flow-sensitive receptors called rapidly adapting receptors;
these are also myelinated, and are primarily sensitive to low
flow rates. During instances of low flow ventilation, these
receptors are stimulated to signal the central controller to upregulate the rate of inspiration.
1.6.2
THE CARDIOVASCULAR SYSTEM
1.6.2.1 Introduction
The key role of the cardiovascular system is to provide all cells
of the body with a continuous stream of oxygen and nutrients
in order to maintain cellular energy transfer. Just as important
a function is the removal of metabolic byproducts from the site
of energy release, which is achieved by cardiovascular circulation. The cardiovascular system involves gas exchange from
lungs to blood and the distribution of this blood around the
body. The following pages present a basic overview of the
cardiovascular system. After reading this section you should be
able to explain: (1) the basic anatomy of the cardiovascular
system, (2) the function and control of the cardiovascular
system, and (3) the process of capillary exchange.
1.6.2.2 Anatomy
The cardiovascular system is made up of a complex and continuous vascular circuit and comprises the following five key
components: the heart, arteries, capillaries, veins, and blood
(Figure 1.6.6). As the name suggests, the heart (cardio) and
the various blood vessels (vascular) are central to the cardiovascular system. The heart provides circulatory blood flow,
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Subclavian artery
Subclavian vein
Cephalic vein
Axillary vein
Axillary artery
Aorta
Superior vena cava
Inferior vena cava
Descending aorta
Branchial artery
Basilic vein
Median cubital vein
Cephalic vein
Ulnar artery
Radial artery
69
Basilar artery
Internal carotid artery
External carotid artery
External jugular vein
Internal jugular vein
Vertebral arteries
Common carotid arteries
Pulmonary arteries
Pulmonary veins
Heart
Celiac trunk
Hepatic vein
Renal veins
Renal artery
Gonadal vein
Gonadal artery
Common iliac vein
Common iliac artery
Internal iliac artery
Palmar digital veins
Digital artery
Internal iliac vein
External iliac vein
External iliac artery
Great saphenous vein
Femoral artery
Femoral vein
Popliteal artery
Popliteal vein
Small saphenous vein
Anterior tibial artery
Posterior tibial artery
Peroneal artery
Anterior/posterior tibial veins
Dorsal venous arch
Dorsal digital vein
Arcuate artery
Dorsal digital arteries
Figure 1.6.6 Schematic of the human cardiovascular system, consisting of the heart and systemic vascular circuit. Dark grey shading represents
oxygen-rich blood, while light grey shading denotes deoxygenated blood
while the vascular provides a network for blood transport. The
arteries make up the high-pressure distribution circuit that
delivers the oxygen-rich blood quickly to the areas in need,
the capillaries are the gas-exchange vessels allowing the diffusion of blood gases and nutrients into and out of the cells,
c06.indd 69
and the veins are the low-pressure collection and return vessels.
An often overlooked but very important part of the cardiovascular system is the blood, which acts as a medium for the
transport of nutrients, wastes, gases, vitamins, and hormones
around the body.
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1.6.2.3
STRENGTH AND CONDITIONING BIOLOGY
The heart
The heart is a hollow and efficient muscular organ which acts
as a pump, providing the thrust required to transport blood
around the body. This pump is situated in the mid-centre of the
chest cavity, about two-thirds of the way to the left of midline.
This four-chamber organ weighs approximately 300–350 g and
is typically about the size of a closed fist. Despite its modest
size and weight, the heart has incredible strength and endurance. At rest, the heart beats approximately 100 000 times per
day, pumping some 4000–5500 L of blood, while the working
heart of an endurance athlete has been calculated to be able to
pump up to 35–40 L in a minute (Powers and Howley, 2007).
The majority of the heart’s mass is composed of muscle; this
muscle, the myocardium, is a form of striated muscle similar to
that of skeletal muscle. In contrast, however, the multinucleated
individual cells or fibres of the heart are shorter than skeletal
muscle and interconnect in latticework fashion via intercalated
discs. These intercellular connections allow electrical impulses
to be transmitted throughout the myocardium, enabling the
heart to function as a single unit (McArdle, Katch and Katch,
2004).
The heart contains four separate chambers or cavities, but
functionally it acts as two separate pumps: the right side of the
heart contains only deoxygenated blood returning from the
body, while the left side contains oxygenated blood returning
from the lungs. The two superior chambers of the heart are
referred to as the right and left atria, while the lower chambers
are the right and left ventricles. During a single cardiac cycle
each chamber in the heart experiences periods of contraction
and relaxation. The relaxation phase where the chamber fills
with blood is called diastole, while the contraction phase where
blood is pushed into an adjacent chamber or arterial trunk is
called systole. Throughout the cardiac cycle circulating blood
from the body enters the heart through the superior and inferior
vena cava and proceeds into the right atrium. During each heart
beat, blood is pumped from the right atrium into the right ventricle. Blood is contained within the right ventricle by a oneway flow valve termed the tricuspid valve, which separates the
right atrium and right ventricle. From the right ventricle, blood
is pumped through the pulmonary artery to the lungs, where gas
exchange occurs. Re-oxygenated blood returning from the
lungs then enters the left atrium through the pulmonary veins.
This blood is pumped into the left ventricle through the bicuspid
valve, which is the term for the atrioventricular valve separating
the left atrium and left ventricle.
tissue, initiates and distributes the electrical impulses responsible for the contraction of cardiac muscle fibres. The sinoatrial
node (SA node) is located on the posterior wall of the right
atrium and is responsible for the spontaneous electrical activity
resulting in myocardial contraction. Due to its role, the SA node
is often termed the natural pacemaker or cardiac pacemaker.
Depolarization of the SA node spreads across the artia, resulting
in atrial contraction. This electrical impulse also depolarizes the
atrioventricular (AV) node, which is located at the inferior floor
of the right atrium. From the AV node, a tract of conducting
fibres called the atrioventricular bundle or bundle of His travels
to the ventricular septum and enters the right and left bundle
branches. These branches diverge into small conduction myofibres called Purkinje fibres, which spread the electrical impulse
throughout the ventricles, resulting in ventricular contraction
(Tortora and Anagnostakos, 1987).
The study of these electrical signals may provide physicians
with valuable information on the function of an individual’s
heart. Such electrical activity can be recorded on an electrocardiogram (ECG) and used to monitor changes or potential problems in heart activity (Figure 1.6.7). Throughout each cardiac
cycle a number of important deflection points may be observed
on a typical ECG trace. The first deflection point is the P wave
and represents depolarization of the atria. The QRS complex
represents the depolarization of the ventricles and the following
T wave represents ventricular repolarisation. Atrial repolarisation is often not observed because it occurs at the same time as
ventricular depolarization and is therefore masked by the QRS
complex. Examination of the magnitude of waves and the time
between deflection points may provide significant information
on the general function of the heart (Tortora and Anagnostakos,
1987).
Stroke volume (SV) refers to the amount of blood ejected
from the left ventricle per contraction. This volume of blood is
R
P-Q
Segment
P
Cardiac function and control
The transfer of blood throughout the heart results from changes
in pressure caused by contracting myocardium. Blood will flow
from one chamber to another only if the pressure gradients
differ. This is important since atria and ventricular pressure
gradients are dependent upon carefully timed muscular contractions. The heart is innervated by the autonomic nervous system
and autonomic neurons may control the rate of cardiac cycle,
though they do not initiate the contraction. Instead, the conducting system of the heart, which comprises specialized muscle
c06.indd 70
S-T
Segment
T
Q
P-R
Interval
S-T Interval
S
QRS
Interval
Q-T Interval
Figure 1.6.7 Example of a resting electrocardiogram detailing the
various phases of the cardiac cycle
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RESPIRATORY AND CARDIOVASCULAR PHYSIOLOGY
simply the difference between the amount of blood present in
the ventricle after filling (end diastolic volume, EDV) and the
volume of blood remaining after ventricular contraction (end
systolic volume, ESV). The proportion of blood ejected with
each beat relative to the filled ventricle (i.e. EDV) is termed the
ejection fraction. The total volume of blood pumped from the
left ventricle each minute is referred to as the cardiac output
(Q). Cardiac output is therefore the product of heart rate (HR)
and stroke volume (SV). Calculations for EF, SV, and Q are
shown below:
EF = (SV EDV ) × 100%
SV = EDV − ESV
Q = HR × SV
Based on the above equation, cardiac output may be altered
by changes in either heart rate or stroke volume. Changing heart
rate is the body’s principal mechanism for short-term changes
in blood supply. Heart rate and stroke volume may be regulated
by many factors, including temperature, emotional state, chemicals, gender, and age. However, the most important control of
heart rate and strength of contraction is the autonomic nervous
system.
Autonomic control
Within the medulla of the brain is a group of neurons called the
cardioacceleratory centre, from which sympathetic fibres travel
down the spinal cord to the heart via the cardiac nerves. When
stimulated, nerve impulses travel from the cardioacceleratory
centre along the sympathetic fibres, causing the release of norepinephrine and resulting in an increase in the rate and strength
of myocardial contraction. Apposing sympathetic tone is parasympathetic stimulus, which also arises from the medulla (cardioinhibitory centre). When this centre is stimulated, electrical
impulses travel along the parasympathetic fibres to the heart via
the vagus nerve, causing the release of acetylcholine, which
decreases heart rate. The control of cardiac output is therefore
the result of apposing sympathetic and parasympathetic tone
(Rowell, 1997). In order to regulate heart rate and strength of
contraction, cardioacceleratory and cardioinhibitory centres are
stimulated in response to changes in blood pressure, which are
detected by baroreceptors located in the carotid artery (carotid
sinus reflex), arch of the aorta (aortic reflex), and the superior
and inferior vena cava (atrial reflex) (Delp and O’Leary, 2004;
Tortora and Anagnostakos, 1987).
1.6.2.4
The vascular system
The vascular system comprises a series of blood vessels which
form a network to transport blood from the heart to the various
tissues of the body, then back to the heart. These vessels differ
in physiological characteristics and function and can be separated into arteries, arterioles, capillaries, venules, and veins.
Arteries are the large, high-pressure vessels that transport blood
c06.indd 71
71
from the heart. Artery walls are constructed of layers of connective tissue and smooth muscle. These vessels are highly
elastic and expand to accommodate the rapid ejection of blood
from the ventricles. When the ventricles relax the elastic arterial
walls recoil, moving blood onwards. Further from the heart,
distributing arteries contain more smooth muscle than elastic
fibres, allowing greater vasoconstriction or vasodilation to regulate blood flow to the periphery. Arteries branch into smaller
vessels called arterioles that deliver blood to the capillaries.
Capillaries are microscopic vessels that permit the exchange
of nutrients and wastes between blood and all cells in the body.
Capillaries are therefore found near every cell in the body,
although the density differs depending on the activity of the
tissue. On average, skeletal muscle contains approximately
2000–3000 capillaries per square millimetre of tissue. A ring of
smooth muscle at the origin of the capillary (pre-capillary
sphincter) controls the regulation of blood flow through a
process termed autoregulation (Delp and O’Leary, 2004;
Wilmore and Costill, 1994).
Dexoygenated blood exiting the capillaries flows into the
venous system through small veins called venules. Venules
transport blood to the veins, from where it is returned to the
heart. Once leaving the capillaries, blood pressure is drastically
reduced. For this reason many veins contain valves that permit
blood to flow in only one direction. Despite this, the low pressure of the venous system results in a considerable volume of
the total blood being contained within the veins (60–65% of
total blood). As such the veins have been referred to as blood
reservoirs. The impact of blood pooling in the veins has received
increasing attention in recent years, with the thought that facilitating venous return will improve the removal of waste products, improving performance and promoting faster recovery
from exercise.
Capillary exchange
The velocity of blood throughout the vascular system is dictated
by the pressure of various vessels. Blood pressure is greatest in
the aorta (100 mmHg) and gradually decreases as it passes
through the arteries (100–40 mmHg), arterioles (40–25 mmHg),
capillaries (25–12 mmHg), venules (12–8 mmHg), veins (10–
5 mmHg), and back to the right atrium (0 mmHg) (McArdle,
Katch and Katch, 2004; Powers and Howley, 2007). Although
pressure gradually decreases, the velocity of blood is lowest at
the capillaries and increases as it enters the venous system. This
increase in velocity is the result of lower peripheral resistance
in venous system. The low velocity of blood through the capillaries is important in allowing the movement of nutrients and
wastes between blood and tissue. The exchange of water and
dissolved substances through capillary walls is dependent on a
number of opposing forces: hydrostatic and osmotic pressure.
Blood hydrostatic pressure (weight of water in blood) tends to
move fluid from capillaries to the interstitial fluid and averages
approximately 30 mmHg at the arterial and 15 mmHg at the
venous end. This flow of fluid is opposed by interstitial fluid
hydrostatic pressure (0 mmHg), tending to move fluid in the
opposite direction. Blood osmotic pressure (28 mmHg) is
related to the presence of non-diffusible proteins in the blood,
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STRENGTH AND CONDITIONING BIOLOGY
which tends to move fluid from the interstitial fluid to the blood.
Opposing this, interstitial fluid osmotic pressure (6 mmHg)
tends to move fluid from capillaries to the interstitial fluid. The
balance between osmotic and hydrostatic pressure dictates the
movement of fluid so that fluid moves from the capillaries to
the interstitial fluid at the arterial end and vice versa at the
venous end (Tortora and Anagnostakos, 1987).
1.6.2.5
Blood and haemodynamics
The blood is a vital part of the cardiovascular system and acts
as a medium for many important functions, including transportation, temperature regulation, and acid–base (pH) balance. The
total volume of blood within an individual’s body typically
ranges from 5 to 6 L in males and 4 to 5 L in females (Wilmore
and Costill, 1994). This blood comprises approximately 55–
60% plasma, with the remainder constituting formed elements.
Plasma is primarily made up of water (∼90%), with the remainder being plasma proteins (∼7%) and cellular nutrients, antibodies, electrolytes, hormones, enzymes, and wastes (∼3%)
(Wilmore and Costill, 1994). The formed elements are the red
blood cells (erythrocytes, 99%), white blood cells (leukocytes),
and platelets (thrombocytes). The ratio between formed elements (i.e. red blood cells) and plasma is referred to as the
haematocrit. Due to reductions in plasma volume, haemoconcentrations may change, resulting in an increase in haematocrit
with little or no change in the total number of red blood cells.
The red blood cells, which make up 99% of the formed elements, have a life span of approximately four weeks and are
responsible for oxygen transportation. Approximately 99% of
the oxygen transported in the blood is chemically bound to
haemoglobin, which is a protein found in red blood cells. Each
red blood cell contains approximately 250 million haemoglobin
Effective
pressure
(–7 mm)
molecules, which may each bind to four oxygen molecules.
Consequently, the oxygen-carrying capacity of blood is
extremely high, with the average healthy male being able to
transport approximately 200 ml of oxygen per litre of blood
when haemoglobin is 100% saturated with oxygen.
The relative saturation of haemoglobin depends upon the
haemoglobin’s affinity for oxygen, which is influenced by a
number of factors, including the partial pressure of oxygen to
which the haemoglobin is exposed (PO2), blood temperature,
pH, and carbon dioxide, carbon monoxide, and 2,3 diphosphoglyceric acid (2–3 DPG) concentrations. The relationship
between oxygen saturation and the PO2 in the blood may be
explained by the oxyhaemoglobin dissociation curve, which is
presented in Figure 1.6.8. This shows that the percentage of
haemoglobin saturation (% HbO2) increases dramatically to a
partial pressure of 40 mmHg, after which it slows to a plateau
of approximately 90–100 mmHg. This relationship is important,
and is responsible for the transportation of O2 from the lungs
to the blood (‘loading’) and from the haemoglobin to the tissue
(‘unloading’). High PO2 in the alveoli of the lungs results in an
increase in arterial O2 pressure and thus the formation of oxyhaemoglobin. In contrast, low PO2 in the tissues deceases capillary PO2, resulting in unloading of O2 and the formation of
deoxyhaemoglobin. At rest, tissue O2 demands are low, resulting in relatively high venous PO2 (40 mmHg), and consequently
only about 25% of the O2 bound to haemoglobin is unloaded to
the tissues. However, with intense exercise PO2 may dramatically drop (18–20 mmHg), resulting in 90% of oxygen being
unloaded (Powers and Howley, 2007). The affinity of oxygen
to haemoglobin may be influenced not only by PO2 but also by
blood pH (Figure 1.6.8). An increase in blood acidity (i.e.
reduction in pH) reduces oxygen’s affinity to haemoglobin by
weakening the bond between them. This influence is referred
to as the Bohr effect and causes an increased unloading of O2
Interstitial fluid
IFHP
BOP
(0 mm) (28 mm)
IFOP
(6 mm)
BHP
(15 mm)
IFHP
BOP
(0 mm) (28 mm)
IFOP
(6 mm)
Venous end
Effective
pressure
(8 mm)
BHP
(30 mm)
Arterial end
Direction of blood flow
Figure 1.6.8 Hydrostatic and osmotic pressures involved in the movement of fluids into the interstitial fluid (out of capillaries; filtration) and
into capillaries (out of interstitial fluid; reabsorption). IFHP = interstitial fluid hydrostatic pressure, IFOP = interstitial fluid osmotic pressure,
BOP = blood osmotic pressure, BHP = blood hydrostatic pressure
c06.indd 72
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CHAPTER 1.6
RESPIRATORY AND CARDIOVASCULAR PHYSIOLOGY
20
100
Volume of O2
unloaded at
tissue
pH 7.60
80
15
pH 7.40
Oxygen Content (ml O2/100 ml blood)
Percent Haemoglobin Saturation (%)
73
pH 7.20
60
10
40
5
20
Arteries
Veins at rest
0
0
0
20
40
60
80
100
Partial Pressure of Oxygen (mmHg)
to the tissues. Likewise, an increase in blood temperature
weakens the bond between O2 and haemoglobin, resulting in
the deoxyhaemoglobin dissociation curve shifting to the right.
Since active tissue produces greater heat and high acid levels
(reduced pH), these shifts facilitate the unloading of O2 to the
active tissue. 2–3 DPG is created by red blood cells during
glycolysis and may bind to haemoglobin, reducing its affinity
for oxygen and enabling unloading of O2 in tissue capillaries
(Powers and Howley, 2007). Concentrations of 2–3 DPG
increase at altitude and in anaemic populations; this is likely to
be an important adaptive mechanism.
At rest the oxygen content in the blood ranges from approximately 20 ml per 100 ml of blood in the arteries to 14 ml per
100 ml of mixed blood in the veins. The difference between
arterial and venous oxygen content is referred to as the arterial
venous oxygen difference (a–v O2 difference) and reflects the
oxygen taken up by active tissue. At rest the a–v O2 difference
is approximately 6 ml (20 : 14 ml), although this may increase
up to 16–18 ml per 100 ml of blood during intense exercise
(Powers and Howley, 2007). This increase in the a–v O2 difference reflects a greater oxygen extraction by the working
tissue (i.e. a decrease in O2 content of venous blood), as seen
in Figure 1.6.9. Throughout exercise the arterial oxygen content
remains relatively stable, although it has been reported to
reduce slightly during high-intensity maximal exercise in elite
athletes, possibly due to blood flow rate exceeding the rate of
oxygen diffusion from alveoli to haemoglobin (red blood cell
transit time) (Chapman, Emery and Stager, 1999; Wilmore and
Costill, 1994).
c06.indd 73
Oxygen Content (ml O2/100 ml blood)
Figure 1.6.9 The relationship between percentage oxyhaemoglobin saturation and partial pressure of oxygen in the blood, known as the
oxyhaemoglobin dissociation curve. Also shown is the influence of pH on haemoglobin affinity for oxygen. Increasing blood temperature has a
similar effect to decreasing pH, resulting in a rightward shift in the curve
20
16
12
a-v O2 diff
8
Arterial O2 content
Venous O2 content
4
1
2
3
4
Oxygen Uptake (L/min)
Figure 1.6.10 Changes in arterial and venous oxygen content during
low to high exercise intensities
The relationship between the a–v O2 difference and the total
volume of blood being pumped to active (i.e. cardiac) tissue
gives an indication of the total oxygen being consumed by the
active tissue (Figure 1.6.10). This oxygen uptake may be
explained by the Fick equation:
VO 2 = Q × (a − v O2 difference )
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1.6.3
CONCLUSION
This chapter reviewed the anatomy, function, and control of the
cardiovascular respiratory system. In particular, it outlined the
c06.indd 74
mechanisms for gas exchange in the lungs, the transportation
of blood in the body, and the exchange of gas and nutrients at
the cellular level.
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1.7 Genetic and Signal Transduction
Aspects of Strength Training
Henning Wackerhage, Arimantas Lionikas, Stuart Gray and Aivaras Ratkevicius, School of Medical Sciences,
College of Life Sciences and Medicine, University of Aberdeen, Aberdeen, UK
1.7.1
GENETICS OF STRENGTH AND
TRAINABILITY
1.7.1.1 Introduction to sport and
exercise genetics
The aim of this chapter is to explain how genetic variation can
influence muscle mass, strength, and trainability, and how
signal transduction pathways mediate the adaptation to strength
or resistance training.
Genetics is the science of heredity; it can be applied to study
exercise-related traits such as strength, maximal oxygen uptake,
and motor skills. Traits such as grip strength depend on both
genetic variation and various environmental factors, or in other
words, nature and nurture. Classical sport and exercise geneticists aim to quantify the genetic contribution to a trait. Why is
this important? There are many answers to this question. For
example, the heritability of a trait informs us whether it is more
dependent on genetically endowed talent or on environmental
factors such as training and nutrition. Also, if a trait’s heritability estimate (heritability can vary between 0 or 0% and 1 or
100%) is high then it makes sense to search for the genetic
variations that explain it.
Heritability has traditionally been estimated by performing
twin or family studies. In twin studies a trait such as grip
strength is measured in monozygotic twin pairs (with identical
DNA) and dizygotic pairs (with 50% shared DNA). The heritability, h2, of hand grip strength can be derived based on the
intraclass correlations (that is, the correlation coefficient, r,
between twin 1 and twin 2 of each pair in the monozygotic
(MZ) and dizygotic (DZ) populations) in the following manner:
h2 = (rMZ − rDZ) / (1 − rDZ) (Newman, Freeman and Holzinger,
1937).
Searching for the genes underlying heritability is a difficult
task because there are over 3 billion base pairs and over 20 000
genes in the human genome. One of the strategies for achieving
this is the candidate gene approach, which is often used when
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
c07.indd 77
an exceptional phenotype is observed. An example where this
strategy has successfully been employed is in a study where
researchers hypothesized that a mutation in the myostatin gene
was responsible for the unusually high muscle mass observed
in a child (Schuelke et al., 2004). The researchers based their
hypothesis on the knowledge that myostatin knockout mice
display hyperplasia and hypertrophy (McPherron, Lawler and
Lee, 1997) and that myostatin mutations occur ‘naturally’ in
some cattle breeds (McPherron and Lee, 1997). After analysing
the myostatin gene in the affected child, the researchers identified a mutation in the myostatin gene which was likely to cause
the phenotype and was not present in the normal population.
Disadvantages of this method are that it only works well with
exceptional, monogenic phenotypes and where a candidate gene
hypothesis can be proposed, for example from a transgenic
mouse model showing a similar phenotype.
Another strategy is to perform so-called genome-wide association studies. In brief, these studies are based on the concept
that variations in relevant genetic markers are associated with
phenotypic variation. Currently a dense set of genomic markers
such as single nucleotide polymorphisms (SNPs) is available.
By studying the effects of each SNP on a phenotype such as
handgrip strength or trainability one can discover genomic
regions that can affect the phenotype.
The advantage of this approach is that, unlike the candidate
gene approach, no prior information on gene function is needed.
This method has the potential to discover novel genes and the
biological pathways that influence a phenotype. The limitation
of this approach is that usually thousands of subjects are needed
for such studies.
1.7.1.2 Heritability of muscle mass,
strength, and strength trainability
In this section we will review the genetic determinants of
muscle mass, strength, and trainability. Muscle mass and
strength depend on environmental factors, such as physical
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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activity, health, and nutrition, and on genetic factors. ‘Genetic
factors’ means that people inherit different alleles or variants
of the genes that affect a trait such as muscle strength. Several
studies indicate that approximately half of the variation in
human muscle strength is inherited (Arden and Spector, 1997;
Carmelli and Reed, 2000; Frederiksen et al., 2002; Perusse
et al., 1987; Reed et al., 1991; Silventoinen et al., 2008; Thomis
et al., 1997).
The physiological mechanism underlying the variation in
strength may be related to the proportion of different fibre
types in skeletal muscle. Slow-twitch (type I) and fast-twitch
(type II) fibres differ in force, power, velocity, rate of relaxation, and fatigability. There is a wide degree of variation in
the proportion of fibre types in specific skeletal muscles. For
example, the proportion of type I fibres ranges from 16% to
97% in human vastus lateralis muscle (Simoneau and Bouchard,
1989; Staron et al., 2000). Due to limitations with human
studies, a wide range of heritability of fibre type proportions
has been reported (Komi et al., 1977; Simoneau and Bouchard,
1995). However, rodent studies provide convincing evidence
of the importance of genetic variation on the proportion of
fibre types (Nimmo, Wilson and Snow, 1985; Suwa, Nakamura
and Katsuta, 1999; van der Laarse, Diegenbach and Maslam,
1984; Vaughan et al., 1974). For example, 37% of fibres in
soleus muscle of the C57BL/6 strain are type I versus 58%
in the CPB-K strain (van der Laarse 1984).
Another physiological mechanism that affects muscle
strength and size is the number of fibres within a given muscle.
For example, Lexell, Taylor and Sjostrom (1988) counted
393 000–903 000 fibres in the vastus lateralis in a cohort of
males with a mean age of 19 years. The design of this study
does not allow quantification of how much of this variation is
due to genetic factors and how much is due to environmental
factors. Animal studies, however, provide evidence that genetic
variation can significantly influence muscle fibre numbers
(Nimmo, Wilson and Snow, 1985; Suwa, Nakamura and
Katsuta, 1999; van der Laarse, Diegenbach and Maslam, 1984;
Vaughan et al., 1974). For example, in population of mice
derived from the C3H/He and SWR strains, heritability of fibres
counted in the soleus muscle was around 50% (Nimmo, Wilson
and Snow, 1985).
Strength and resistance training is the main method utilized
to increase both muscle mass and strength. Individuals vary in
their ability to adapt to strength training, or in other words their
strength trainability differs. A study carried out on more than
500 young, untrained, healthy individuals confirmed that the
same strength training programme results in greatly varying
strength and muscle size adaptations (Hubal et al., 2005). After
12 weeks of progressive resistance training the elbow flexor
strength increased on average by 54%, and muscle size by 19%.
However, the extent of change varied from 0% to +250% for
strength and from −2% to +59% for muscle size (Hubal et al.,
2005).
Why does strength trainability vary that much? The answer
is unknown, but a potential explanation is again the variation
in the proportion of fast- and slow-twitch fibres. Several studies
c07.indd 78
report that type II fibres hypertrophy to a greater extent than
type I fibres in response to strength training (Hather et al.,
1991; Houston et al., 1983; MacDougall et al., 1980; Staron
et al., 1990). Thus individuals with more type II fibres may
experience a greater muscle hypertrophy after a strength training programme than individuals with more type I fibres.
Another possible explanation is that allelic variation of the
genes relevant for the adaptive response to training per se
plays an important role. A twin study examining the role of
the genetic factors on strength gain following resistance training showed that ∼20% of variation in strength gain after
training is explained by the genetic variation in trainability
and is not related to variation at the baseline (Thomis et al.,
1998).
To summarize, muscle strength in a population varies due
to genetic and environmental factors affecting the development
and maintenance of skeletal muscle and also because of genetic
factors that affect the adaptation to external stimuli such as
strength training. Many questions remain, including ‘What and
how many genetic variants have a significant effect on
strength?’, ‘What is the effect size of genetic variants?’, and
‘What is the frequency of these genetic variants in different
populations?’ Answers to these questions are needed in order
to allow us to develop meaningful applications such as genetic
tests to predict strength or strength trainability.
Mutations in a single gene can disrupt the function of the
coded protein or preclude its translation affecting the phenotype in a profound way and even causing disease. Duchenne
muscular dystrophy is an example of such a disease.
Understanding the heredity of such conditions enabled
accurate predictions of whether the mutant allele, if inherited,
would result in disease. This led to expectations that variation
in a phenotype such as strength might be affected in a similar
manner, where allelic variant of some major gene determines
whether strength-generating ability is high or low. Such a
scenario, however, is rare. For example, allelic variants of
the ACTN3 (Walsh et al., 2008) and CNTF (Roth et al.,
2001) genes, implicated in variation in muscle strength, exerted
rather small effects, accounting for ∼1% of phenotypic
variation.
In the polygenic model of genetic effects, many genes
together influence the phenotype through a small effect of
each. Studies on skeletal muscle in mice support the polygenic
model in strength as a number of the genomic regions known
as quantitative trait loci (QTL), which affect muscle mass,
were identified on different chromosomes of the mouse genome
(Brockmann et al., 1998; Lionikas et al., 2003; Masinde
et al., 2002). Identification of the genes underlying these QTL
will offer researchers new candidate genes and biological pathways for examination of their effects on human muscles; this
will eventually lead to identification of the genes underlying
high heritability estimates and understanding of the constellations of alleles resulting in high or low muscle strength. Even
while the underlying genes remain elusive, acknowledgement
of the polygenic nature of the genetic effects is important
because it means that predictions of strength performance for
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79
1.7.2 SIGNAL TRANSDUCTION
PATHWAYS THAT MEDIATE THE
ADAPTATION TO STRENGTH TRAINING
an individual based on his or her alleles of one gene are of a
very limited value.
Genetic testing is currently accessible to the general public
(Genetic Technologies Ltd, 2007). It is often assumed that
such tests can predict athletic ability. Perhaps the most popular
gene offered for testing is ACTN3. It has been discovered
that mutation in this gene resulting in a premature stop codon
is common in Caucasians (North et al., 1999). It was also
noted that the frequency of the mutant X allele, which encodes
the stop codon, among elite power athletes is lower and
among endurance athletes higher than in the general population (Yang et al., 2003). While a genetic test can determine
the alleles of ACTN3 carried by an individual, the predictive
value of such information is limited because the gene accounts
only for ∼1% of strength variation (Walsh et al., 2008).
Testing with a genetic test for a single gene effect will not
provide much information. One can however envisage that
in the future useful information may be obtained by testing
for multiple genes which all affect, for example, muscle
power. At present screening for 50 m sprinting ability, vertical
jumps, or 1 RM strength tests is a more informative assessment of athletic potential. Ethical and legal implications also
have to be taken into account when deciding whether or not
to perform genetic tests on athletes. This has been reviewed
as part of the BASES position stand on ‘Genetic Research
and Testing in Sport and Exercise Science’ (Williams et al.,
2009).
1.7.2.1 Introduction to adaptation
to exercise: signal transduction
pathway regulation
In the last 20 years exercise physiologists have used molecular
biology techniques to address the question ‘What are the mechanisms that make skeletal muscle and other organs adapt to
exercise?’ The answer is: signal transduction pathways. Such
pathways:
1. sense signals associated with exercise via sensor proteins;
2. integrate this information, often by kinase-mediated phosphorylation and phosphatase-mediated dephosphorylation,
as well as other forms of protein–protein interaction;
3. regulate the transcription and translation (protein synthesis)
of genes, or other functions such as protein breakdown, cell
division, and cell death (Figure 1.7.1).
We will now explain these three steps. Sensor proteins are
comparable to sensor organs such as the eye, ear, and nose.
Exercise
Exercise
signals
SE
(1)
(2)
(4)
(3)
TF
mRNA
Transcription
SP P
TR P
P
TF P
mRNA
(5)
Protein
Translation
Other cell
functions
Nucleus
Figure 1.7.1 Model detailing adaptation to exercise. (1) Exercise changes many intra- and extracellular signals, which are sensed by sensor
proteins (SE). (2) This information is then conveyed and integrated by a network of signalling proteins (SPs). (3) These signalling proteins
regulate functions such as transcription, where a gene is copied into mRNA, (4) translation, which is the synthesis of new protein from mRNA,
which takes place in ribosomes, and (5) other cell functions such as cell division. Transcription is regulated by DNA-binding transcription factors
(TF) whereas translation is regulated by translational regulators (TR)
c07.indd 79
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Table 1.7.1 Five sensor proteins
Sensor protein
Binding sites for
Mediates adaption to
AMPK
AMP, glycogen
HIF prolylhydroxylases
calmodulin
adrenergic
receptors
titin kinase
oxygen
increased energy
turnover
hypoxia
calcium
adrenaline
force/stretcha
muscle contraction
systemic exercise
changes
passive muscle stretch
a
Stretch increases ATP binding to titin kinase, which primes the enzyme
for subsequent autophosphorylation (Puchner et al., 2008).
late the mRNAs into proteins and make a cell grow. Other
proteins regulate protein breakdown, the activity and location
of transporter proteins such as glucose transporters, the synthesis of new DNA, or the aggregation of DNA to chromosomes
before and during cell division and even cellular death.
1.7.2.2 Human protein synthesis and
breakdown after exercise
After resistance exercise, signal transduction pathways regulate
changes in protein synthesis and breakdown. Before discussing
the signalling pathways involved we will first focus on these
downstream effects. A positive protein balance (net protein
accretion) is essential for muscle growth:
net protein accretion = protein synthesis − protein breakdown
During strength training many molecules bind to the sensor
proteins and variables such as force, temperature, and length
change are sensed intracellularly by them. These small molecules will change the conformation and/or activity of the sensor
proteins and thus trigger a signalling cascade. Table 1.7.1 gives
five examples of sensor proteins.
One can imagine how ‘rest’ signals (low AMP, high glycogen, low calcium, low adrenaline, low force/stretch) differ from
‘exercise’ signals (high AMP, low glycogen, high calcium, high
adrenaline, high force/stretch) and how consequently a unique
set of signalling proteins is activated by exercise.
Signalling proteins, like the nervous system, convey the
information gathered by the sensor proteins, compute it, and
regulate outputs. The main class of signalling proteins are proteins that can use a phosphate group from an ATP to phosphorylate or dephosphorylate a serine, threonine, or tyrosine on one
or more downstream proteins. The enzymes that phosphorylate
proteins are termed ‘kinases’ while those which dephosphorylate proteins are termed ‘phosphatases’. There are 518 kinase
genes in the human genome (Manning et al., 2002) and a similar
number of phosphatases. Apart from phosphorylation, proteins
can also be ubiquitinated, sumoylated, acetylated, and hydroxylated (this list is incomplete) affecting the activity, stability,
localization, and/or protein–protein interactions of the downstream protein.
The resultant system is a network of thousands of signalling
and auxiliary proteins. This network, similar to the network of
neurons in the brain, not only conveys information linearly from
sensor proteins to the downstream endpoints, but also computes
such information. A good example of this is the AMPK–mTOR
signalling network, which senses and computes signals such as
AMP, glycogen, amino acids, and muscle loading to regulate
protein synthesis and ribosome biogenesis. The AMPK–mTOR
system will be discussed in more detail below.
At the bottom of the cellular signalling network are proteins
that regulate nearly all cellular functions such as transcription
factors and translational regulators. Transcription factors bind
to DNA binding sites and recruit RNA polymerase to genes
whose transcription is up- or downregulated by exercise.
Translational regulators assemble ribosomes, which then trans-
c07.indd 80
A positive protein balance can occur through an increase in
protein synthesis, a decrease in protein breakdown, or any combination of the two that results in net protein accretion.
Throughout daily life there is a continuous turnover of protein
within skeletal muscle, with synthesis and breakdown both
occurring at varying levels depending on age, nutritional status,
and contractile activity. During exercise, both resistance and
endurance, the majority of ATP is used in the development of
force and power within the muscle. This means that many other
‘non-essential cellular processes’, including protein synthesis,
are reduced during the initial recovery period after exercise. The
reduction of protein synthesis during acute muscle contraction
was first observed in a perfused rat hindlimb (Bylund-Fellenius
et al., 1984).
After resistance exercise, once contraction-related ATP
requirements are back to basal levels, there is a marked increase
in protein synthesis. Depending on the intensity at which exercise is performed, protein synthesis will be approximately
doubled 12–24 hours after exercise (Chesley et al., 1992), followed by a slow decrease. Even 72 hours after exercise, muscle
protein synthesis can still be higher than before exercise (Miller
et al., 2005). The duration of this period of elevated protein
synthesis has been found to be longer in untrained compared to
trained subjects (Phillips et al., 1999). In response to a lower
intensity of contractile activity there is a slight increase in
protein synthesis, but this is generally short-lived. This doseresponse relationship between muscle protein synthesis and
exercise intensity has recently been characterized in both young
(24 ± 6 years) and old (70 ± 5 years) subjects. Kumar et al.
(2009) measured muscle protein synthesis 1–2 hours after exercise and found that in both young and old subjects there is a
sigmoidal relationship between exercise intensity and muscle
protein synthesis (Figure 1.7.2). The protein synthesis response
was consistently smaller in the older population. One major
finding of this study was that exercise intensities above 60% 1
RM were required for protein synthesis to be maximized. This
indirectly supports strength training practice (ACSM, 2009).
These data also make sense in light of a meta-analysis that
showed that resistance training with 60% of 1 RM in untrained
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CHAPTER 1.7
GENETIC AND SIGNAL TRANSDUCTION ASPECTS OF STRENGTH TRAINING
Figure 1.7.2 Dose–response relationship of myofibrillar protein
synthesis (FSR, fractional synthetic rate, % h−1), measured at 1–2 h
post-exercise for five young men (24 ± 6 years) and five older men
(70 ± 5 years) at each intensity. Reproduced from Kumar et al.
(2009) with permission from Blackwell Publishing
subjects and 80% of 1 RM in trained subjects is most effective
at increasing muscle strength (Rhea et al., 2003).
We mentioned previously that protein breakdown must also
be taken into account when looking at protein accretion within
the muscles. Intuitively one might think that resistance training
decreases protein breakdown to stimulate additional growth, but
in reality this is probably not the case. It appears that protein
breakdown is not altered during exercise (Tipton et al., 1999)
but, like protein synthesis, is elevated after resistance exercise
in fasted subjects (Biolo et al., 1995). The magnitude of this
increase is approximately 25–50%, peaking approximately 3
hours after exercise, leaving the muscles in a slightly improved
(compared to rest) but still negative protein balance. The duration of the increase in muscle protein breakdown is believed
to be shorter than that observed for protein synthesis (Phillips
et al., 1997). In order to achieve a positive protein balance a
meal needs to be ingested, as this will elevate protein synthesis
above breakdown (Tipton et al., 1999).
1.7.2.3 The AMPK–mTOR system and
the regulation of protein synthesis
The AMPK–mTOR signalling system is now well established
as the major regulator of protein synthesis in response to resistance exercise. Several practical implications arise from our
understanding of this system. The AMPK–mTOR system and
myostatin signalling are shown in Figure 1.7.3.
The mTOR pathway is a complicated pathway which regulates the assembly of the ribosome and the subsequent synthesis
of proteins, which is also known as translation. mTOR forms
two complexes with other proteins, termed mTORC1 and
mTORC2 (Proud, 2007). The mTOR pathway not only stimulates many steps that lead to an upregulation of protein synthesis
c07.indd 81
81
(Proud, 2007) but also regulates the capacity for protein synthesis by producing more ribosomes, which are the cellular
machines that synthesize proteins (Mayer and Grummt, 2006).
We will not discuss this pathway in detail, but will focus on
those elements and functions that are important in regulating
the adaptation of skeletal muscle to resistance exercise.
The first evidence of the involvement of the mTOR pathway
in mediating the growth adaptation to resistance exercise was
obtained by studying high-frequency electrically stimulated rat
muscles. Using this model it was demonstrated that p70 S6k,
which is downstream of mTOR, was increasingly phosphorylated after high-intensity stimulation and that the activity of
p70 S6k correlated with the magnitude of muscle growth (Baar
and Esser, 1999). It was later shown that mTOR was necessary
for muscle hypertrophy (Bodine et al., 2001a) and that the PKB/
Akt-mTOR signalling cascade was activated in response to
IGF-1 (a known muscle growth factor) signalling (Rommel et
al., 2001). A considerable amount of evidence has been accumulated to support the hypothesis that IGF-1 splice variants
play a key role in stimulating muscle hypertrophy after resistance exercise by activating the mTOR pathway (Goldspink,
2005). However, recent mechanistic studies have cast doubts
on the importance of IGF-1 and suggest that mTOR activation
after resistance exercise is instead dependent on phospholipase
D (PLD) (O’Neil et al., 2009). The exact signal that activates
mTOR after resistance exercise in a PLD-dependent or possibly
independent manner is currently unknown. One candidate
sensor is titin kinase (Lange et al., 2005), where a stretch/forcesensing mechanism has been identified (Puchner et al., 2008).
The mTOR pathway is also activated by nutrients, which has
important implications for whether and when nutrients should
be taken by athletes engaging in resistance exercise. The mediators of the nutrient response are insulin and essential amino
acids, especially leucine. Like IGF-1, insulin activates mTOR
via receptors and PKB/Akt, but the mechanism by which amino
acids activate mTOR is still not entirely known. It probably
involves small GTPase proteins (Avruch et al., 2009).
AMPK is a kinase that is activated by elevated AMP which
increases during exercise and triggers the upstream kinases to
phosphorylate AMPK at Thr172 and inhibited by glycogen
(Wojtaszewski et al., 2002). The activation of AMPK by high
AMP and low glycogen is dependent on AMP and glycogen
binding sites on AMPK subunits (Hudson et al., 2003). AMPK
not only regulates many acute and chronic adaptations to
endurance exercise but also inhibits translation initiation and
elongation via TSC2 (Inoki, Zhu and Guan, 2003) and eEF2
(Horman et al., 2002). In other words, AMPK activity reduces
protein synthesis and muscle growth, and this mechanism can
explain the reduction of protein synthesis during acute exercise
(Bylund-Fellenius et al., 1984). Many studies suggest that
AMPK does indeed inhibit translational signalling, protein
synthesis, and growth in skeletal muscle (Bolster et al., 2002;
Dreyer et al., 2006; Thomson, Fick and Gordon, 2008), but
a recent study suggests that it may not always be involved
(Rose et al., 2009). One can imagine a tug of war where
protein synthesis is reduced via AMPK and increased via
mTOR.
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?
IGF-1, insulin
Amino acids
PLD
(1)
mTOR
(3)
AMPK
P
TR P
AMP
Glycogen
(2)
P
Transcription
(4)
Smad P
mRNA
mRNA
Protein
Translation
Nucleus
Myostatin ↓
Figure 1.7.3 Model detailing adaptation to exercise. (1) mTOR is activated by resistance exercise via phospholipase D (PLD), amino acids, and
endocrine factors such as IGF-1 (although changes in IGF-1 are probably not required for the adaptation to resistance exercise) and insulin.
(2) mTOR then activates translation factors, resulting in increased translation initiation and elongation of protein synthesis. (3) mTOR is
inhibited by AMPK, which is activated by an increase in the concentration of AMP and by a low glycogen concentration. Thus endurance
exercise and low glycogen due to exercise or diet will inhibit mTOR and protein synthesis. (4) Myostatin expression usually decreases after
resistance exercise. This results in decreased Smad2/3 phosphorylation, translocation to the nucleus, and decreased muscle-growth inhibitory
gene expression. Details and references are given in the text
1.7.2.4
Potential practical implications
To summarize, mTOR and protein synthesis are more active
when AMP is low, glycogen is high, after resistance exercise,
and when nutrient uptake leads to increased concentrations of
amino acids and insulin. What are the practical implications?
Concurrent endurance and strength
training where muscle hypertrophy is
the goal
Hickson reported that combined strength and endurance training led to less strength increase over 10 weeks than strength
training alone (Baar, 2006; Hickson, 1980). Assuming that the
decreased strength increase in the strength and endurance training group was due to less hypertrophy, this can be explained
by the inhibition of protein synthesis by AMPK and/or other
mechanisms. So what can be done for sports such as rowing or
rugby where muscle mass, strength, and endurance need to be
developed in parallel? Judging purely from the signalling data,
strength training for muscle hypertrophy should be avoided
when muscle glycogen is low. Thus, especially after highintensity endurance exercise where glycogen is nearly depleted
after 20 minutes or after >1 hour of medium intensity exercise
(Gollnick, Piehl and Saltin, 1974), it will probably be important
c07.indd 82
to increase the glycogen content before engaging in resistance
exercise for hypertrophy. This is because of the likely inhibition
of protein synthesis by low glycogen. Also, prolonged coolingdown exercise should be avoided for the muscles that have been
strength trained due to the AMPK activation.
Concurrent endurance and strength
training where muscle hypertrophy
is not a goal
In other sports, such as boxing or Alpine climbing, endurance
and strength have to be increased but muscle mass and body
weight gains need to be minimized. A potential strategy here is
to increase AMPK activity during or after resistance exercise
to minimize the growth response but to maintain the neuromuscular adaptation to exercise. Potential strategies to reduce the
growth effect of resistance exercise are to avoid protein or
amino acid intake before, during, and directly after resistance
exercise, as these would increase the growth response (Esmarck
et al., 2001; Tipton et al., 2001). Also, performing endurance
exercise and especially glycogen-depleting types of exercise
(Gollnick, Piehl and Saltin, 1974) before or shortly after resistance exercise will activate AMPK and should thus reduce the
growth response more than exercise that is performed well after
resistance exercise.
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CHAPTER 1.7
1.7.2.5
GENETIC AND SIGNAL TRANSDUCTION ASPECTS OF STRENGTH TRAINING
Myostatin–Smad signalling
The counterpart of the mTOR pathway is the myostatin–Smad
system. Its key component is a muscle-secreted protein or
myokine that has been termed ‘myostatin’. Myostatin is a
member of the transforming growth factor-β (TGF-β) family
(Lee, 2004; McPherron, Lawler and Lee, 1997) and inhibits
muscle growth. Myostatin knockout mice have a 2–3 times
higher muscle mass than the wildtype due to both hyperplasia
and hypertrophy of muscle fibres. Various natural mutations of
the myostatin gene have been reported. These include muscular
cattle breeds such as the Belgian Blue or Piedmontese
(McPherron and Lee, 1997) and a human mutation (Schuelke
et al., 2004). In contrast, overexpression of myostatin causes
cachexia in mice (Zimmers et al., 2002).
Expression of myostatin mRNA can be detected pre- and
postnatally. It is regulated by environmental stimuli: most (Roth
et al., 2003; Walker et al., 2004; Zambon et al., 2003) but
not all (Willoughby, 2004) studies show that resistance and
endurance exercise reduce myostatin mRNA and/or protein.
In contrast, myostatin expression increases in response to
muscle immobilization (Wehling, Cai and Tidball, 2000).
Glucocorticoids also promote the transcription of myostatin
(Ma et al., 2001).
Myostatin is expressed as a larger precursor protein that is
cut to yield functionally active ∼24 kDa myostatin dimers (Lee,
2004). After secretion, myostatin can bind and be neutralized
by serum proteins such as growth and differentiation factorassociated serum protein-1 (gasp1), follistatin, and follistatinrelated gene (FLRG) (Lee, 2004). Thus, myostatin signalling
depends not only on the concentration of myostatin protein but
also on its processing and the availability of inhibitory binding
partners. Active myostatin binds to activin IIA and IIB receptors (Lee and McPherron, 2001), which then recruit and phosporylate activin type I receptors, increasing their kinase activity.
The type I receptor phosphorylates the receptor-regulated
Smads (R-Smads), Smad2 and Smad3 (Bogdanovich et al.,
2002). This activated complex of R-Smads dissociates from the
receptor and binds to the common Smad, termed Smad4. The
Smad complexes translocate to the nucleus and bind to short
DNA stretches termed ‘Smad-binding elements’ and regulate
the expression of hundreds of genes (Massague, Seoane and
Wotton, 2005). Myostatin inhibits the proliferation and differentiation of mononucleated cells, such as satellite cells, which
are important for muscle fibre formation and regeneration
(Thomas et al., 2000). It is unclear how a decrease in myostatin
signalling promotes muscle growth in adult muscle. Hypertrophy
requires a positive protein balance and there is little information
on the effect of myostatin on protein synthesis or breakdown.
To our knowledge only one in vitro study has demonstrated an
inhibition of protein synthesis by myostatin and this was in a
muscle cell culture model (Taylor et al., 2001).
Myostatin inhibitors are potential treatments for muscle
atrophy in disease and ageing but may equally be misused as
doping agents. Anti-myostatin antibodies have been used to
successfully improve muscle function in a mouse model of
muscular dystrophy (Bogdanovich et al., 2002). The myostatin
c07.indd 83
83
Smad system has advantages for drug developers as it can be
targeted extracellularly and as is a muscle-specific signalling
protein. A study where a monoclonal anti-myostatin MYO-029
antibody was used in muscular dystrophy patients has been
completed but no significant muscle size or other treatment
effects have been reported (Wagner et al., 2008). In another
study, single muscle fibre contractile properties were improved
in patients who received MYO-029, but the patient numbers
(n = 5) and controls (n = 1) were small (Krivickas, Walsh and
Amato, 2009)
To summarize, myostatin is the opponent of mTOR signalling when it comes to controlling of muscle growth. Myostatin
expression is regulated by environmental sitmuli such as exercise but it is largely unclear how reduced myostatin signalling
promotes hypertrophy.
1.7.2.6 Signalling associated with
muscle protein breakdown
Skeletal muscle protein breakdown occurs through a number
of different proteolytic pathways. Proteolysis can be simple
defined as the process in which proteins, in this case myofibrillar proteins, are broken down into peptides or amino acids by
cellular enzymes called proteases. In skeletal muscle these
pathways include lysosomes, ubiquitin-proteasome-dependant
systems, calcium-activated proteases, caspases, and metalloproteinases. The precise role of each mechanism in the skeletal
muscle adaptations associated with exercise remains to be fully
elucidated. Indeed only a handful of studies have investigated
changes in these systems during exercise.
The muscle-specific ubiquitin ligases muscle atrophy F box
(MAFbx) and muscle-specific really-interesting novel gene
finger protein 1 (MuRF-1) have been implicated in the control
of protein breakdown, with both sharing forkhead box 3A
(FOXO3A) as a transcription factor. Indeed, in cell culture
overexpression of MAFbx results in fibres of a smaller diameter
and in mice with both MAFbx and MuRF-1 genes knockout
demonstrate atrophy sparing when the sciatic nerve is cut
(Bodine et al., 2001b). Similarly, when FOXO3A is constitutively active in myotubes it activates MAFbx transcription,
resulting in a reduction in fibre diameter (Sandri et al., 2004).
In response to resistance exercise, MAFbx and MuRF-1 have
been found to be rapidly elevated, with a suppression of MAFbx
and FOXO3A 4–24 hours after exercise (Louis et al., 2007;
Raue et al., 2007). Further studies have also found that MAFbx
mRNA was decreased for up to 24 hours after a bout of resistance exercise (Kostek et al., 2007), indicating that it may not
be involved in the upregulation of muscle protein breakdown
in response to exercise. Further support for such an assertion
was found by Greenhaff et al. (2008), who discovered that
MAFbx was not associated with changes in protein breakdown.
Clearly the involvement of these ubiquitin ligases in the control
of protein breakdown during exercise remains to be
elucidated.
Further studies have demonstrated that increasing intracellular Ca2+ concentration in skeletal muscles, ex vivo, will lead
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to an increase in protein breakdown (Baracos, Greenberg and
Goldberg, 1986; Goodman, 1987; Kameyama and Etlinger,
1979; Zeman et al., 1985). From these findings a logical
hypothesis would be that stimulation of protein breakdown
via Ca2+ would occur through the Ca2+-activated proteases.
However, in testing this hypothesis recent work has found that
calpains, Ca2+-activated proteases, are not activated in skeletal
muscle during exercise (Murphy, Snow and Lamb, 2006). A
final mechanism was suggested in 1984 when it was demonstrated by Bylund-Fellenius et al. (1984) that in muscles in
which protein breakdown was inhibited there was a degradation
of high-energy phosphates and an accumulation of lactate. This
led the authors to conclude that protein degradation might be
linked to the energy status of the muscle and the level of metabolite accumulation.
It appears unlikely, therefore, that one single pathway controls the rapid remodelling of myofibrillar proteins after a bout
of exercise, but rather that multiple pathways probably contribute to various degrees.
1.7.2.7 Satellite-cell regulation during
strength training
Skeletal muscle fibres are multinucleated cells with many hundreds of nuclei in each myofibre, each of which has a volume
of cytoplasm, or the so-called nuclear domain. It has been
hypothesized that the ratio between a nucleus and the volume
of muscle fibre is relatively constant. Indeed, there is a parallel
increase in both muscle fibre volume and nuclear number in
response to functional overload in rats (Roy et al., 1999),
meaning that the nuclear domain will remain relatively constant. It has been suggested that in humans there is a ceiling
size to the myonuclear domain of around 2000 μm2, after which
no growth of the myofibre is possible (Kadi et al., 2004). In
that case it is only possible for the skeletal muscle to grow with
the addition of further nuclei, which poses a problem as skeletal
muscle cells are post-mitotic (do not divide anymore) and thus
external cells must provide these additional nuclei.
Satellite cells are skeletal muscle-specific stem cells and
are found between the basal lamina and the cell membrane of
each myofibre (Mauro, 1961). Satellite cells play a major role
in the regulation of muscle development, postnatal growth, and
injury repair (Kuang, Gillespie and Rudnicki, 2008), and potentially in the hypertrophy response to exercise (Rosenblatt
and Parry, 1993), although this is not universally accepted
(O’Connor and Pavlath, 2007). Evidence supporting the role
of satellite cells in hypertrophy includes the findings that satellite cells proliferate, and re-enter the cell cycle, in response to
various hypertrophic stimuli, including synergistic ablation,
stretch overload, testosterone, and importantly resistance exercise. For example, markers of satellite-cell activation and cellcycle activity, such as cyclin D1, and of differentiation, such
as p21 and MyoD, are increased after a single bout of resistance exercise (Bickel et al., 2005) and more prolonged strength
training (Kadi et al., 2004). The time course of satellite-cell
proliferation lasts from approximately 1–2 days after resistance
c07.indd 84
exercise up to a week, which is before any significant increase
in myofibre size will occur. In order to investigate the physiological significance of the increase in satellite cell numbers,
various studies have used local gamma irradiation to inhibit
satellite-cell function, with the classical study being performed
by Rosenblatt and Parry (1993). After such treatment hypertrophy is either completely prevented or drastically reduced in
response to a hypertrophic signal, suggesting a role for satellite
cells in hypertrophy, depending upon the stimuli applied.
Furthermore, in response to disuse during spaceflight, immobilization, hind-limb suspension, denervation, and ageing, the
number of myonuclei in a single muscle fibre decreases, due
to death by apoptosis, highlighting a likely role for satellite
cells in atrophy as well as hypertrophy. On the other hand, as
mentioned above, several studies have indicated that hypertrophy is possible without the activation of satellite cells. These
studies have used pharmacological β-adrenergic agonists,
which have an anabolic effect in skeletal muscle, finding that
an increase in muscle size/mass or protein content occurs
without any changes in DNA content (a surrogate for muscle
nuclei). In order to fully resolve the inconsistencies in these
findings and reveal the true role of satellite cells in skeletal
muscle hypertrophy, more advanced methods will need to be
developed to determine whether satellite-cell fusion is necessary for skeletal muscle hypertrophy.
1.7.2.8 What we have not covered
Due to a lack of space we have had to leave out important
molecular mechanisms that link skeletal muscle and other
organs to strength and the adaptation to strength training. Here
we briefly mention these mechanisms to give an idea of the
larger picture.
Besides skeletal muscle, the major strength and strengthadaptation organ is the nervous system. It controls the number
of contracting muscle fibres by activating α-motor neurones
and thus motor units, and the intensity of fibre contraction by
regulating the discharge rate of motor units in response to training (Duchateau, Semmler and Enoka, 2006). The cause for such
neural adaptations is unclear but it seems likely that it will
involve genes that are regulated by neuronal activity and which
consequently change synapse or neuron behaviour (Flavell and
Greenberg, 2008). The double challenge for researchers in this
field is to identify the mechanisms responsible for such behaviour in the complex nervous system and to explore the complex
signalling within the cells therein.
Finally, bones and tendons adapt to resistance exercise in
a manner similar to skeletal muscle. In bone the challenge is
to identify the signal transduction pathways that link mechanical signals associated with bone loading with increases in collagen synthesis and tissue mineralization (Scott et al., 2008).
Tendons adapt to exercise via an increase in collagen synthesis
and modifications of the proteins at the extracellular matrix
(Kjaer et al., 2005). Again, signal transduction pathways link
exercise to these processes, and these remain to be fully
elucidated.
10/18/2010 5:11:26 PM
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GENETIC AND SIGNAL TRANSDUCTION ASPECTS OF STRENGTH TRAINING
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1.8 Strength and Conditioning
Biomechanics
Robert U. Newton, School of Exercise, Biomedical and Health Sciences, Edith Cowan University, Joondalup,
WA, Australia
1.8.1
INTRODUCTION
Biomechanics is the science of applying mechanical principles
to biological systems such as the human body. As such biomechanics has much to offer the field of strength and conditioning. A basic knowledge of biomechanics is essential
for the specialist involved in testing and training people because
mechanical principles dictate the production of movement
and the outcomes in terms of performance. Strength and
conditioning methods often involve both simple and quite
complex equipment and apparatus which the athlete will
manipulate and interact with. These interactions and subsequent
demands placed on the athlete’s neuromuscular system are
determined by biomechanical principles. As we will see, the
human body is constructed of a series of biological machines
that allow us to produce an incredible range of movement
and the resulting sport, training, dance, and everyday activities. For the sake of simplicity, some of the biomechanical
concepts will be explained with slight variations from the
strict mechanical definitions. In the strength and conditioning
field it is more important to convey meaning and for the
concepts to be understood than to be pedantic about the
terminology.
The purpose of this chapter is to convey some key biomechanical concepts essential for understanding how we produce
movement, how various exercise machines function and interact with the performer, and how tests and equipment are used
to assess performance.
1.8.1.1
Biomechanics and sport
All sporting movement results from the application of forces
generated by the athlete’s muscles working the bony levers and
other machines of the skeletal system. Human movement is
incredibly complex in all the myriad activities in which we
participate, and this is perhaps most eloquently expressed in
the extraordinary exploits of athletes. For example, jumping
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
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vertically into the air is a common movement that most of us
perform without thought, but the underlying mechanical phenomena which contribute to jumping are numerous and
complex. Understanding and application of biomechanics is
integral to the strength and conditioning specialist and will
make for more effective and safer exercise programme designs.
This process occurs at several levels:
1. Biomechanics knowledge increases understanding of how a
particular movement is performed and the key factors that
limit performance.
2. A major aspect is technique analysis because greater movement understanding brings better ability to identify inefficient and/or dangerous techniques.
3. The range of equipment available for strength and conditioning is considerable and expanding. Biomechanical analysis
will differentiate useful and well-designed equipment from
that which is potentially dangerous or undesirable.
Understanding of biomechanics also permits the design of
new equipment and exercises based in science.
4. From a biomechanical perspective the athlete can be examined as a machine with neural control and feedback, mechanical actuators, biological structures with certain properties,
and interaction with the environment and equipment. This
brings excellent understanding of factors limiting performance and mechanisms of injury. The result is better training
programme design.
1.8.2 BIOMECHANICAL CONCEPTS
FOR STRENGTH AND CONDITIONING
It is important to develop a basic understanding of some key
mechanical variables and relationships so that we can explore
in more detail biomechanical concepts of strength and conditioning exercise, performance testing, and test interpretation.
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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1.8.2.1 Time, distance, velocity,
and acceleration
Time
We all experience the passing of time in the fact that we remember what we have just experienced and know that events will
occur in the future. Time is measured in various units, but
principally seconds, minutes, hours, days, months, and years are
used in strength and conditioning to represent different quantities of time. For very short events time is usually measured in
milliseconds.
Units of measurement are often the result of equations used to
calculate the quantity. For example, velocity is displacement
divided by time and so has units of m/s, or more commonly
m.s−1. The dot between the m and the s means product or multiplication, while the −1 superscript to the seconds means
inverse or 1 over seconds. They are the same units, just
expressed differently mathematically.
1.8.2.2 Mass, force, gravity,
momentum, work, and power
Distance
Mass
Distance is a slightly different mechanical quantity to displacement but the terms are usually used interchangeably. In strength
and conditioning we usually refer to the length of a path over
which a body or an object moves, and this is correctly termed
‘distance’. Distance is a measure of a change in position or
location in space and has two forms, linear and angular. Linear
distance is usually measured in metres (m) and is the length
of the path travelled. Angular distance refers to how far an
object has rotated and is normally measured in degrees. You
may also see angular distance measured in radians. A radian
is equal to approximately 57°. Displacement is not always
the length of the path taken but rather is the length of a
straight line between the initial and final position. We can
illustrate the distinction between the two terms using the bench
press. When lowering the barbell to the chest and returning
the arms to the extended position the initial and final position
are the same, so the displacement of the barbell is zero.
Distance is the length of path down and up, so will be say
1.6 m.
The quantity of matter that makes up a given object. This
sounds a quite abstract concept but fortunately it is easy to
measure because we often equate mass with weight. The two
concepts are not the same, because weight is actually the force
generated by gravity (defined below) acting on the mass. Mass
is measured in units of kilograms (kg).
Velocity
Velocity (often termed speed) is the rate of change of distance
over time. It is calculated as the distance moved divided by the
time taken to cover that distance and is expressed in units of
metres per second (m/s).
Inertia
The resistance of an object to changes in its state of motion. In
other words, if the object is stationary it will resist being moved;
if it is already moving it will resist changes in the direction or
speed of movement. Inertia in linear terms is measured in kilograms and is functionally the same as mass. For example, a
sprinting football player who weighs 120 kg is much harder to
stop than a gymnast who weighs 50 kg.
Force
Force can be most easily visualized as a push or pull for linear
force or a twist for rotating force (termed torque). Force is
measured in units called Newtons (N), or Newton metres (N.m)
in the case of torque. To produce a change in motion (acceleration) there must be application of a force or torque. The amount
of change that results depends on the inertia of the object. To
calculate the total force of resistance at a given time point the
following formula is used:
F = m (a + g )
Acceleration
Acceleration is the rate of change of velocity with time. It refers
not only to changes in rate of movement but also to changes in
direction. The change of running direction when performing a
cutting manoeuvre requires an acceleration other than zero,
even though the speed of movement might be maintained.
Acceleration is calculated as the change in velocity divided by
the time over which this occurred. The measurement unit is
usually metres per second per second (m/s/s).
It should be noted that both velocity and acceleration refer
not just to linear motion but also to angular motion or
rotation.
The units of measurement of these physics quantities are
defined according to established standards called the International System of Units, abbreviated as ‘SI units’. All of the
countries of the world except three (Burma, Liberia, and the
United States) have adopted SI as their system of measurement.
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where F = force, m = mass of barbell or dumbbell, a = instantaneous acceleration, g = acceleration due to gravity (9.81 m/s/s).
Torque is calculated as the force applied multiplied by the
length of the lever arm:
T=F×d
As an example, a 10 kg weight placed on the ankles 0.5 m
from the centre of the knee joint and with the lower leg (shank)
parallel to the floor creates a 10 × 9.81 × 0.5 = 49.05 N.m of
torque about the knee.
Gravity
A specific force produced because of the enormous size of the
planet Earth. Simply because of the mass of the Earth there is
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an attractive force on all objects near to it, and that is why when
you throw a ball into the air it falls back to the ground. The
most common form of resistance training uses this principle:
weight training is lifting and lowering objects against the force
of gravity.
Momentum
The quantity of motion that an object possesses, momentum is
calculated as the velocity multiplied by the mass. The units are
kilogram metres per second (kg.m/s). This concept has relevance to strength and conditioning across a range of aspects,
including injury mechanisms and assessment of performance.
For example, it is often useful to express sprinting ability not
just in terms of time or velocity but in terms of momentum.
This is because an athlete with mass 100 kg running at 10 m/s
has considerably more momentum than an 80 kg athlete running
at the same velocity. In collision sports such as rugby or football
it is momentum that usually determines the outcome. Momentum
is also important to consider during resistance training because
the load that is applied to the athlete is not simply the mass but
also how fast the weight is moving.
Impulse
The product of the force applied and the time over which this
force is acting. The units of measurement are Newton seconds
(N.s). This is a very important parameter for strength and conditioning because of what has been termed the impulse–
momentum relationship. For most athletic movements,
achieving a high velocity of release (in jumping, sprinting,
throwing, kicking, striking) is a critical performance outcome.
This velocity is determined entirely by the impulse imparted to
the body, ball, or implement. As an example, the velocity of
takeoff in the vertical jump and thus the resulting jump height
is the result of the impulse that the athlete can apply to the
ground.
Work
Calculated as the force applied multiplied by the distance
moved. It is a useful concept in strength and conditioning. For
example, in coaching, the volume of a weight-training workout
is most accurately calculated as the amount of work completed.
Work is measured in units called joules (J).
Power
The rate of doing work, power can be calculated as work divided
by the time over which it is completed. Power can also be calculated as the force applied multiplied by the velocity. Power is
measured in units called Watts (W), although it is also frequently expressed in horsepower (hp), whereby 1 hp = 745.7 W.
1.8.2.3
Friction
Friction is the force that resists two surfaces sliding over each
other. The concept is important for strength and conditioning
because we use friction in exercise equipment (e.g. weighted
sled towing), and it is also a factor in weight training (e.g.
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STRENGTH AND CONDITIONING BIOMECHANICS
91
chalk applied to hands). Friction is a force and so is measured
in Newtons. It is related to the nature of the two surfaces and
the force pressing them together; it should be noted that it is
the interaction between both surfaces. For example, a smoothsoled basketball shoe has excellent grip on the polished wooden
floor of the court but little grip when used on a grassed soccer
field. An example which illustrates how increasing the force
pushing two surfaces together affects friction is the Monarch
cycle ergometer, which is commonly used for exercise testing
and training. When you adjust the tension on the belt around
the wheel, the belt is pushed harder on to the wheel rim,
increasing friction and thus the exertion required to push the
pedals.
1.8.3
THE FORCE–VELOCITY–POWER
RELATIONSHIP
Most sports require the application of maximal power output
rather than force. Understanding the mechanical quantity of
power and factors contributing to its generation is invaluable to
the strength and conditioning specialist. Due to the structure of
muscle and how it lengthens and shortens while developing
tension, the amount of force that can be produced is related to
the velocity at which the muscle is changing length (Figure
1.8.1). The following discussion assumes that the muscle is
being maximally activated. Several important points for strength
and conditioning arise from this phenomenon:
1. The lowest tension can be developed during concentric
(shortening) contractions.
2. When the velocity is zero, this is termed an isometric contraction, whereby the muscle is generating tension but
no movement is occurring. Greater tension is developed
during isometric contractions than during concentric
contractions.
Force (F/Fmax) and Power (P/Pmax)
CHAPTER 1.8
Fmax
Pmax
Power
Force
eccentric
0.0
concentric
Velocity (V/Vmax)
Vmax
Figure 1.8.1 Force–velocity–power relationship for muscle
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3. Negative velocities indicate that the muscle is lengthening
while developing tension; this is termed eccentric. Muscle
can generate greatest tension while it is lengthening. Note
that at faster velocities of lengthening the force no longer
increases and may even decrease slightly, most likely due to
reflex inhibition.
4. Positive power can only be produced during concentric contractions and the faster the velocity of muscle shortening, the
less force the muscle can develop. When the muscle is contracting against a high external load, force is high but velocity will be low. If the load is light then high contraction
velocity can be achieved but force is low. Because of this
interplay of force and velocity, the product of the two is
maximized at a point in between. In fact, power output is
greatest when the muscle is shortening at about 30% of the
maximum shortening velocity. This by definition corresponds to a force of approximately 30% of that produced
during an isometric contraction.
We observe this phenomenon regularly in the weight room.
For example, when squatting heavier loads, the speed of movement decreases. For maximal lifts the velocity may be very low,
in fact it might approach zero in certain phases of the range of
motion as the lifter tries to maximize the force applied. Also,
when performing training aimed at increasing power output,
lighter loads tend to be used, but moved at much higher velocities, say 30–50% of isometric maximum.
1.8.4
MUSCULOSKELETAL MACHINES
The muscles develop tension and this is applied to the bones to
produce or resist movement. Essentially these systems are a
form of machine, taking the tension developed by the muscle
and converting it to motion of a bone around a joint. There are
many examples of such machines in the human body and when
accurately controlled by the computer which is our nervous
system the result is the bewildering array of human movements
that we observe each day. In this case the musculoskeletal
machines function to change high force production and small
range of muscle length change into low force but high velocity
and range of motion at the end of the bone opposite that to
which the muscle attaches.
1.8.4.1 Lever systems
The most common musculoskeletal machine in the body is the
lever system. The muscle pulls on the bone, which may rotate
about the joint. A lever is a common machine in everyday use
(using a screwdriver to open a can of paint, a tyre lever to
dislodge a hubcap). In these examples, the length of the force
arm is much greater than that of the resistance arm and so
pushing on the lever with say 100 N results in 1000 N applied
on the paint lid to push it open (Figure 1.8.2). But note that the
handle end of the screwdriver must move through 10× the
B
A
humerus
muscle force
large force
finish position
small force
long path
fulcrum
short path
ulnar
start position
Figure 1.8.2 Examples of basic lever systems designed for high range and speed of movement (a) or high force (b). For the elbow flexion (a),
note that a small shortening of the muscle results in a large displacement at the hand, however much higher force is required by the muscle to
produce force at the hand. In (b), a long lever is used to move a heavy object. A large range of movement and less force at the long end results
in high force but limited range of movement applied to the object being moved
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CHAPTER 1.8
class of
lever
STRENGTH AND CONDITIONING BIOMECHANICS
1st
2nd
3rd
F
R
E
E
E
E
F
F
examples triceps extending the
elbow
F
R
R
R
93
rising up on the ball of
the foot
Lifting a dumbbell
with elbow flexion
Figure 1.8.3 Arrangement of fulcrum, effort, and resistance for the three different classes of lever
distance of the blade end under the lid. This tradeoff of distance
and force is called mechanical advantage. Interestingly, the
musculoskeletal machines of the human body usually work at
a mechanical disadvantage in terms of force but advantage in
terms of distance moved and thus velocity capability: we are
designed for speed rather than high force production (Figure
1.8.2).
There are three possible types of lever and all of these can
be observed in the human body. Class of lever is based on the
arrangement of the fulcrum (F; pivot point or joint), resistance
(R; point of application of force against the resistance), and
effort (E; muscle attachment and thus point of application of
the muscle force). A good way to remember the three classes
of lever is ‘FRE’ (Figure 1.8.3). In a first-class lever, the
fulcrum (F) is in the middle. In a second-class lever the resistance (R) is in the middle. In a third-class lever the effort (E) is
in the middle. In the human body, the third-class lever is the
most common because it is the best design for large range and
speed of motion. First-class is the next most common because
depending on whether the fulcrum is closer to the effort or the
resistance, first-class levers can favour either force production
or range of motion. Second-class levers are the least common
in the human because such an arrangement always results in
mechanical advantage and thus reduced speed and range of
motion. Remember, we are designed for speed and range of
motion – not force production.
1.8.4.2
Wheel-axle systems
Wheel-axle machines only occur at ball and socket joints; the
hip and shoulder are particularly important examples and are
commonly involved in strength and conditioning. When either
of these joints is moving in internal or external rotation the
muscles and bones are working as a wheel-axle system. When
the tendon of the agonist muscle wraps partially around the end
of the bone, muscle tension will tend to rotate the bone about
its long axis, similar to the axle in an automobile.
Let’s examine the example of the shoulder joint being internally rotated. The tendon of the pectoralis major muscle inserts
c08.indd 93
on the humerus, and when the shoulder is externally rotated the
tendon is partially wrapped around the bone. Muscle shortening
internally rotates the humerus, forearm, and hand. If the elbow
is flexed, the hand will travel through a much greater distance
than the upper arm, and hence the system acts as a machine,
trading force production at the proximal end of the humerus for
greater distance and velocity of movement at the hand.
1.8.5
BIOMECHANICS OF MUSCLE
FUNCTION
A number of key aspects of how muscle functions are important
for understanding the biomechanics of strength and conditioning. Force or power applied is determined by a complex range
of neural and mechanical interactions within the muscle,
between muscle and tendon, and between muscle and the
machines of the skeleton.
1.8.5.1 Length–tension effect
Muscle generates tension by the interaction of myosin and actin
filaments; this process results in the muscle being able to generate different quantities of tension at varying lengths. This is
termed the length–tension effect, which is an inverted ‘U’ relationship such that greatest tension is produced when the muscle
is at or near its resting length, and substantially less contractile
tension can be developed when the muscle is stretched or shortened above or below this length (Figure 1.8.4). The actual force
output of the muscle is slightly different to this because as the
muscle stretches beyond the resting length another force
increases in contribution: the elastic recoil of the stretched
muscle and tendon (Figure 1.8.4).
1.8.5.2 Muscle angle of pull
Muscles pull on the bones to produce movement, resist movement, or maintain a certain body position. This force acting on
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the bony levers generates torque. The muscle force is most
efficiently converted to torque when the angle at which the force
is applied is at 90° to the long axis of the bone. At angles other
than perpendicular, only a portion of the muscle force is directed
to producing joint rotation, with the remainder tending to either
pull the joint together (stabilizing force) or apart (dislocating
force) (Figure 1.8.5). Muscle angle of pull has a very large
impact on the effectiveness of the developed muscle tension.
For example, when the angle of pull is 30° to the long axis of
the bony lever, the contractile force is only 50% efficient in
terms of transfer into torque about the joint.
total tension
1.8.5.3 Strength curve
tension
100% of resting
contractile tension
elastic tension
muscle length
Figure 1.8.4 Length–tension effect for skeletal muscle, showing
both contractile tension and elastic components
A
Combination of the length–tension effect and angle of pull
results in the strength curve for the particular movement. It
is important to note that the strength curve is the net combination of all the muscles, bones, and joints involved in the movement: for a single joint movement, such as elbow extension,
only the triceps brachii length and angle of pull combine to
produce the strength curve; for a more complex, multijoint
movement, such as bench press, all the muscles involved in
shoulder horizontal adduction and elbow extension combine
to produce the strength curve. The result is a range of differentshaped strength curves for each movement. The most common
is ‘ascending’, which describes movements such as squat and
bench press. In both cases, from the bottom to the top of the
lift the force-generating capacity of the musculo-skeletal
system increases.
B
C
percentage of muscle force
100
80
60
40
20
0
0
20
40
60
80 100 120 140 160 180
muscle angle of pull
Figure 1.8.5 Muscle angle of pull determines percentage of muscle force contributing to joint rotation (solid line) or to dislocating and
stabilizing forces (dashed line). (a) Angle of pull is less than 90° and dislocating force is evident. (b) Angle of pull is 90° and 100% of muscle
force is contributing to joint rotation, with no dislocating or stabilizing force. (c) Angle of pull is greater than 90° and a stabilizing force is evident
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STRENGTH AND CONDITIONING BIOMECHANICS
95
Figure 1.8.6 Line of resistance for the arm curl. The white arrow represents the resistance vector and the red arrow represents the component
producing torque about the joint. The length of the red arrow indicates the amount of resistance force applied. Note that the resistance torque is
maximized when the forearm is horizontal and is considerably less at higher or lower angles
1.8.5.4 Line and magnitude
of resistance
The direction of the force that must be overcome during resistance training is termed the line of resistance. When training
with free weights this is always vertically down because the
resistance is the gravitational weight force acting on the barbell
or dumbbell. Using combinations of levers and pulleys, the line
of resistance for a given exercise can be in any direction. For
example, for a pull-down machine, a pulley is used to reverse
the direction of the downwards gravitational force of the weight
stack to provide a vertically upward force. Similarly, pulleys
are used in a seated row machine to direct the line of resistance
horizontally (Figure 1.8.6).
For essentially linear movements such as squat, shoulder
and bench press, the resistance of a free weight stays constant
except for changes in velocity. This is because, as we have
already seen, force is equal to mass times (a + g). The result is
that when the velocity of movement is constant, acceleration is
zero, and so the resistance is simply the weight force of the
barbell. However, when increasing velocity at the start of the
lift (positive acceleration) the resistance to overcome is higher
than the weight force alone. At the top of the lift, when velocity
is decreasing (negative acceleration), the resistance to overcome is actually less than the weight force of the barbell.
The changes in magnitude of resistance become even more
complex for rotational movements such as arm curls or knee
extensions with free weights. The resistance torque about the
joint will change in a sine wave fashion so that it is greatest
when the limb is horizontal and zero when the limb is vertical.
1.8.5.5
Sticking region
Combining the strength curve with the line of resistance for a
given movement results in varying degree of difficulty through
c08.indd 95
the range of motion. So even though the external resistance
might be constant, some parts of the lift are more difficult than
others. This is termed the ‘sticking region’ and is the point in
the movement at which the lift is most likely to fail. For
example, in a standing elbow flexion (arm curl) exercise using
a dumbell, the sticking region is around 90–110° joint angle.
Interestingly, this is a region of high torque capability in the
strength curve, but it is also where the resistive torque generated
by the dumbbell is at its peak. For the bench press, the sticking
region is 5–10 cm off the chest. This is a linear lift and the line
and magnitude of resistance do not change appreciably.
However, at this point the strength curve is at a low point due
to inefficient angle of pull for the pectoralis major. Also, at this
point the initial high force generated at the changeover from
eccentric to concentric phases has dissipated (see Section 1.8.8)
and mechanical advantage has not yet started to increase
appreciably.
1.8.5.6 Muscle architecture, strength,
and power
Muscles in the human body have a range of designs or architectures specific to the functional demands required. The two
main divisions are fusiform and pennate, and each has several
subtypes. Fusiform muscles (e.g. biceps brachialis) have muscle
fibres and fascicles running in parallel to a tendon at origin and
insertion, longer fibre length, and are able to generate good
range of shortening and in particular higher velocity of shortening. The architecture of pennate muscles involves muscle fibres
running obliquely into the tendon. Such a structure allows more
muscle fibres to be packed into the muscle and this favours
higher force output.
The angle at which the muscle fibres are aligned relative to
the tendon is termed the pennation angle and this also has
impact on the relative ability of the muscle in terms of force
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versus shortening velocity. A higher pennation angle favours
force production, while a lower angle allows the muscle to
produce greater range of motion and velocity of contraction.
It is important for the strength and conditioning specialist to
understand the concepts of muscle architecture and pennation
angle due to their implications for function and thus performance. Of particular interest is the fact that pennation angle can
be altered through training. For example, Blazevich et al.
(2003) have demonstrated changes in muscle pennation angle
in as little as 5 weeks of resistance training. Heavy resistance
training leads to an increase in pennation angle and thus
increased strength capacity. Higher-velocity ballistic training
produces adaptations of decreased pennation angle and thus
increased velocity and power output. The fact that such changes
occur in as little as 5 weeks of training has considerable importance for the periodization of training programme design.
1.8.5.7 Multiarticulate muscles, active
and passive insufficiency
Many muscles of the body are multiarticulate: they cross more
than one joint and therefore can produce movement at each of
the joints they cross. This arrangement has great benefits in
terms of efficiency and effectiveness of muscle contraction.
However, there are two considerations for strength and conditioning. A muscle can only shorten by a certain amount, typically up to 50% of its resting length. The result is that if the
muscle is already shortened about one joint then it cannot contract very forcefully to produce movement over the other joint
that it crosses. This is termed ‘active insufficiency’ and has
significance for resistance training. In selecting certain exercises, one can change the emphasis on a given muscle group.
For example, when training the calf muscles, ankle plantar
flexion can be performed with the knee extended (standing calf
raise) or flexed (seated calf raise), switching the training emphasis from the gastrocnemius to the soleus. In a standing calf raise
the gastrocnemius is lengthened over the knee joint and so is the
primary muscle producing the ankle plantar flexion. However,
in a seated calf raise the gastrocnemius is already shortened
about the knee joint and cannot contribute much force about the
ankle. The soleus becomes the prime mover in this case.
Similarly, a muscle can only be stretched to a certain extent.
Multiarticulate muscles are lengthened over all the joints they
cross. If a given muscle is already in a lengthened state to allow
movement to the end of the range for one joint then it may not
be possible to lengthen it further to permit full range of motion
at the other joint it crosses. This is termed ‘passive insufficiency’. For an application of this principle to exercise we will
again use the gastrocnemius and soleus. To adequately stretch
the muscles of the calf one has to perform two stretches: one
with the knee extended, which tends to place the gastrocnemius
on stretch, and the other with the knee bent to stretch the soleus.
As soon as you bend the knee, the gastrocnemius is no longer
fully lengthened about the knee and so can allow more dorsiflexion of the ankle. The soleus then becomes the limiting
muscle and so is effectively stretched.
c08.indd 96
1.8.6 BODY SIZE, SHAPE, AND
POWER-TO-WEIGHT RATIO
Consideration of body size and shape is important to understanding individual differences in strength and power. For
example, long trunk and short arms and legs favours powerlifting and weightlifting performance because the shorter lever
lengths permit greater force production if all else is equal.
However, fast speed of movement (e.g. throwing or kicking) is
better achieved by an athlete who has longer relative limb
lengths. In general, the larger the athlete’s body size and mass,
the greater their strength capability because absolute strength is
very much dependent on total muscle mass and cross-sectional
area. In many sports, relative strength and power are more
important than absolute measures. These measures are the
strength-to-weight and power-to-weight ratio, respectively, and
are simple measures to calculate. For example, relative strength
for a given movement is simply the 1RM divided by body mass.
If we assume a 1RM squat of 120 kg at a body mass of 80 kg
the relative strength for this movement is 1.5. In any sport in
which projection of the body is important (e.g. vertical jumping,
sprinting) the power-to-weight ratio of the athlete is a critical
measure because it determines the amount of acceleration and
thus peak velocity that can be achieved. For example, an athlete
who produced 6000 W in a vertical jump at a body mass of
100 kg has a power-to-weight ratio of 60 W/kg.
The centre of mass (COM) is that point about which all of
the matter of the body is evenly distributed in all directions.
When standing upright with the arms at the sides in the anatomical position this point is in the middle of the abdomen, just
below the navel. The human body can move and take all manner
of positions and so the COM also moves and can even lie
outside the body. The concept of COM becomes important
when discussing balance and stability.
1.8.7
BALANCE AND STABILITY
It is useful to have an understanding of the biomechanics of
balance and stability when analysing strength and conditioning
movements. Balance is the process of controlling the body position and movements in either static or dynamic equilibrium for
a given purpose. Stability is the ease or difficulty with which
this equilibrium can be disturbed. Because all exercises require
balance, manipulating stability can impact the degree of difficulty and injury risk, or can be used to introduce a different
training stimulus, for example balance training.
1.8.7.1 Factors contributing to stability
Stability is determined by:
1. Base of support: the physical dimensions of the area defined
by the points of support. For example, when performing
the military press exercise the base of support is the area
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97
defined by the rectangle enclosing both feet. If the feet are
placed further apart then the base of support is larger and
stability is higher. If the split position is adopted, the area
increases even further, particularly in the anterior–posterior
plane (Figure 1.8.7). When seated on a bench with the feet
wide apart the area and thus stability is even greater.
2. Mass of the object or body: heavier objects are inherently
more stable because the inertia (resistance to change in state
of motion) is higher, as is the gravitational weight force. For
example, placing weight plates on a Smith machine or power
rack makes the device more stable.
3. Height of the COM: as noted above, for a human standing
with their arms at their sides, the COM is in the centre of
the body, roughly 5 cm below the navel. Raising their arms
over their head lifts the COM; bending at their hips and
knees lowers it. The higher the COM, the less stable the
object.
4. Location of the COM relative to the edges of the base of
support: if a line dropped down from the COM is close to
an edge of the base of support the body will have low stability in that direction.
With this knowledge the strength and conditioning specialist
can alter the body position and the equipment used to increase
or decrease stability. For example, if an older person is having
difficulty maintaining balance while performing arm curls then
seating them on a bench will make the exercise easier. This is
because the base of support has been increased and the COM
lowered. If an athlete is unstable when performing the triceps
press down exercise, spreading the feet and splitting them one
forward and one back, bending slightly at the knees, will give
much better stability. There are also instances where less stability is desirable to increase the balance demands of the task. This
can be achieved for the dumbbell shoulder press, for example,
simply by standing on one leg.
1.8.7.2 Initiating movement or change
of motion
When an athlete attempts to accelerate quickly or change direction, they will decrease their stability in the direction of movement. This means any given force they exert in that direction
will result in rapid acceleration. For example, in starting the
sprint, the athlete leans as far forward over the hands so that
the line of gravity (straight line down from the COM) falls very
close to the front edge of their base of support.
1.8.8
THE STRETCH–SHORTENING
CYCLE
Almost all human movement involves a preparatory or ‘windup’
action in the opposing direction, followed by the intended
movement. This sequence involves a lengthening and stretching
c08.indd 97
Figure 1.8.7 Base of support for standing feet spread (narrow and
wide stance) versus split position. Shifting from narrow to wide
stance greatly increases stability in the side-to-side directions.
Moving to the split position increases stability in the forward and
backward directions
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of the muscles used to produce the movement, followed by a
shortening, and so has been termed the stretch–shortening cycle
(SSC). This phenomenon is important in strength and conditioning because such an action is performed to some extent in
all training exercises. In fact, some exercises such as plyometrics are designed specifically to develop SSC ability. The preparatory movement involves eccentric muscle contraction and
this phase potentiates the subsequent concentric movement by
around 15–20%. That is, movements performed without a prestretching produce 15–20% less impulse than true SSC movements. There are around six mechanisms proposed (Walshe
et al. 1998) to explain this phenomenon, but the predominant
factor is that a higher level of force (termed ‘pre-load’) can be
generated at the start of the concentric movement if prestretching is performed. Although the stretch reflex and storage
and recovery of elastic strain energy have also frequently been
touted, the role of these two mechanisms is probably less important, particularly in short-duration ballistic movements such as
squat, vertical jump, and throwing.
movement the acceleration is negative and the resistance to
overcome is actually reduced. This contributes to why the top
part of a squat or bench press requires less effort than earlier in
the concentric phase.
1.8.9.2 Gravity-based machines
A disadvantage of free weights is that the line of resistance is
always vertically downwards. A second problem is that the
resistance (that is, the weight force of the dumbell or barbell)
is constant. This does not match the strength curves for various
movements and as such the amount of weight that can be lifted
is limited to that which can be successfully moved through the
sticking region previously discussed. For this reason several
machines have been developed, all using the gravitational
weight force but modifying the resistance curve to more closely
match the strength curve for the movement. The biomechanics
of these techniques will be discussed shortly.
Pulleys
1.8.9 BIOMECHANICS OF
RESISTANCE MACHINES
The variety of equipment developed for strength and conditioning is quite remarkable. This equipment is all designed to
change the direction of resistance and in some cases vary the
magnitude of resistance through the range of movement. Most
use the gravitational weight force but there is also a plethora of
machines that use elastic, hydraulic, aerodynamic drag, or
pneumatic resistance. How these machines interact with the
human body is determined by biomechanical principles. While
some have been well designed, others have not incorporated
good biomechanics and the result has been poor effectiveness
or even injury risk. Understanding the mechanics underlying a
piece of resistance training or conditioning equipment will
assist in initial purchase decisions as well as exercise selection.
Following is a discussion of the predominant resistance machine
designs.
1.8.9.1
Free weights
Working against the inertia and gravitational weight force of a
freely moving mass such as a dumbell or barbell represents the
most simple but perhaps most frequently used form of resistance training. The biomechanics of such equipment are similarly straightforward, with the resistance acting vertically
downward at all times. The force can be calculated as F = mg,
where m = the mass and g = acceleration due to gravity
(9.81 m/s/s). When the weight is also being accelerated there is
an additional resistance due to the inertia of the object and this
extra force can be calculated as F = ma. For rapid movements
this component of the resistance to movement can become quite
large, for example in the clean and jerk or snatch. As already
described, when the weight is decreasing in velocity of
c08.indd 98
The most basic modification was to build machines which
allowed the weight force to be redirected. Early versions
used standard weight plates but then incorporated cables and
pulleys to provide vertically upward or horizontally directed
resistance.
Pin-loaded
To overcome the problems of shifting weight plates on and off
these early machines, a weight stack was incorporated, with a
pin used to select the resistance. This improved ease of use,
helped to keep the weight room tidier, and reduced injury risk
from lifting weight plates on and off the machines.
Levers and cams
The next problem to overcome was the mismatch of the resistance profile to the strength curve for the movement. For
example, in the bench press using free weights or constant
resistance machines the load lifted is limited to what can be
moved through the bottom part of the range. Once the load is
off the chest, the effort required decreases as the ascending
strength curve exceeds the constant resistance load by an
increasing proportion. In this scenario, the neuromuscular
system is not stressed as much in the upper part of the range of
motion and the intensity is limited by the sticking region. To
overcome this problem a range of variable resistance devices
were developed. The initial designs involved sliding levers; an
example was the universal variable resistance. The principle
was simple: as bench- or leg-press movement proceeded from
the bottom to the top position, the lever arm would slide out,
changing the point of application of the load on the weight
stack, increasing the moment arm and thus the amount of resistance to be overcome by the lifter.
Later examples used variable radius cams, for example
Nautilus, to achieve the same result. In this case a cable or chain
wrapping around a cam with a changing radius altered the
length of the resistance arm and thus the amount of resistance
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CHAPTER 1.8
STRENGTH AND CONDITIONING BIOMECHANICS
that the lifter must overcome. Using biomechanical principles
the cams could be designed to match the strength curve for
various training exercises.
One of the most recent implementations of the variable
resistance concept in resistance training is the Hammerstrength
range of equipment. The biomechanics of this equipment is
quite simple and effective. The weight plates are placed on
horns located at the end of a lever. In the bottom position the
lever is rotated out of the vertical position, and as in the concepts we discussed earlier regarding line of resistance, not all
of the weight force of the plates is directed against the lifter.
As the lift is executed, the lever arm moves toward the horizontal and so the vertically downwards weight force moves closer
to 90° to the lever arm and the amount of load transferred to
the lifter increases, matching more closely to the strength curve
for the movement.
1.8.9.3
Hydraulic resistance
Hydraulic resistance devices use a hydraulic ram and the resistance of oil (hydraulic fluid) being forced though a small
aperture. Two different technologies are used. One involves
flow control; the size of the aperture is adjusted, thus changing
99
the velocity at which the fluid can flow and therefore the
speed of movement. As greater force is exerted against the
machine the resistance increases to match as the fluid is incompressible and velocity of flow is somewhat independent of
the pressure. The second type uses a pressure-release valve
configuration. The valve is initially held closed by a tensioned
spring but when a force greater than the valve resistance is
applied the valve opens and the fluid is permitted to flow.
This technology provides a more constant resistance, similar
to free weights, compared to the quasi-constant velocity of
flow-control systems.
It is important to note that both systems are passive and thus
provide a purely concentric exercise mode. This equipment has
found a niche in circuit training programme designs and with
special populations because there is reduced muscle soreness
(no eccentric phase), it is easy to use, and no momentum is built
up, thus reducing the risk of injury.
1.8.9.4 Pneumatic resistance
As the name suggests, this equipment uses air pressure (pneumatic) to provide resistance to both concentric and eccentric
exercise. A pneumatic ram similar to an enormous syringe is
Table 1.8.1 Biomechanical comparison of machines versus free weights
Free Weights
Lower stability means greater balance control required; this may
have added training effect
Line of resistance is constant and vertically downward
Resistance force is constant and proportional to the mass, and
does not necessarily match the strength curve for a specific
movement
Resistance is more specific to the free masses that must usually be
manipulated in sport performance and tasks of everyday living
While free weights do not match strength curves, their free,
three-dimensional movement does allow for wide variation in
weight, height, lever length, and gender
Lifting free weights, particularly in a standing position, requires
considerable activation of muscles acting as fixators and
stabilizers, which increases training efficiency and strengthens
muscles in these important roles
Both eccentric and concentric phases of free-weight lifts can
generate considerable momentum, which must be controlled at
the end of range by the lifter to avoid injury
Require more effort loading the bar, lifting plates on and off,
lifting barbells and dumbbells from the rack; all may be a
source of injury if not performed with good ergonomics
Not a biomechanical issue, but administratively free weights
require more effort to keep orderly and tidy
If the lifter cannot complete a lift, some exercises such as bench
and squat are difficult to escape from under the bar
c08.indd 99
Machines
Higher stability makes exercise easier for novices and certain
populations where demands of balance control may be risky or
compromise strength gains
Line of resistance can be altered to any plane and direction
Resistance force can be varied through the use of levers and cams
in an attempt to match strength curve
Controlling the plane of movement, varying the resistance, and
changing the line of resistance reduces specificity of training
Even the best application of biomechanics can only approximate
the average person, and deviations in height, weight, gender,
and lever lengths result in a considerable mismatch of machine
and body mechanics
While less activation of muscles other than the agonists is required
when using machines, this allows concentration on the agonist
muscles for greater activation
Machines, and in particular hydraulic and pneumatic machines,
reduce the amount of momentum generated; training may be
safer in this aspect
Load is easily selected and changed
Easy to keep tidy and safe exercise environment
Weight stack just drops back and stops if lifter cannot fails the
attempt
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STRENGTH AND CONDITIONING BIOLOGY
preloaded to a certain pressure using compressed air. The higher
the pressure, the greater the resistance provided. When the
movement is performed, the ram compresses the air even
further, increasing pressure and thus resistance. This provides
an ascending resistance curve, which matches reasonably well
the ascending strength curve of most human movements. On
the return movement the athlete is working to control the speed
of the expanding gas and so these machines allow eccentric as
well as concentric phases.
1.8.9.5
Elastic resistance
Examples range from equipment as simple as the theraband to
devices such as the Vertimax. All use the resistance that is
developed when an elastic material such as rubber or bungee
cord is stretched. Such devices also provide an ascending resistance curve because elastic tension is greater the more the material is deformed, and they allow for eccentric exercise as the
muscles act to control the speed of elastic recoil.
c08.indd 100
1.8.10
MACHINES VS FREE WEIGHTS
It is an interesting biomechanical discussion to compare the
advantages and disadvantages of machines versus free weights
for resistance training. Clearly each has benefits and it is really
a matter of understanding the different biomechanical principles and then selecting the equipment and exercises appropriate
to the individual. An evaluation is included in Table 1.8.1.
1.8.11
CONCLUSION
Biomechanics has considerable application in understanding
many aspects of strength and conditioning. From an appreciation of the determinants of friction and how an athlete can
develop force against the ground, to the design principles of the
wide array of resistance equipment available, biomechanics
knowledge will enable the strength and conditioning professional to increase their effectiveness and safety.
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CHAPTER 1.8
References
Blazevich A.J., Gill N.D., Bronks R. and Newton R.U. (2003)
Training-specific muscle architecture adaptation after 5-wk
training in athletes. Medicine & Science in Sports &
Exercise, 35 (12), 2013–2022.
c08.indd 101
STRENGTH AND CONDITIONING BIOMECHANICS
101
Walshe A.D., Wilson G.J. and Ettema G.J. (1998) Stretchshorten cycle compared with isometric preload:
contributions to enhanced muscular performance. Journal
of Applied Physiology, 84, 97–106.
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c08.indd 102
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Section 2
Physiological adaptations to
strength and conditioning
c09.indd 103
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c09.indd 104
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2.1 Neural Adaptations to
Resistance Exercise
Per Aagaard, University of Southern Denmark, Institute of Sports Science and Clinical Biomechanics,
Odense, Denmark
2.1.1
INTRODUCTION
Resistance training induces adaptive changes in the morphology and architecture of human skeletal muscle while also
leading to adaptive changes in nervous system function. In
turn, all these changes appear to contribute to the marked
increase in maximal contractile muscle force and power that
can be seen with resistance (strength) training in both young
and ageing persons, including even very frail and old (>80
years) individuals. The adaptive change in neural function
has been evaluated by use of muscle electromyography (EMG)
measurements, which recently have included single motor
unit recording and measurements of evoked spinal reflex
responses (Hoffman reflex, V-wave) and transcranial brain
stimulation (TMS, TES). Also, interpolated muscle twitch
recording superimposed on to maximal muscle contraction
has been used to assess the magnitude of central activation
of the muscle fibres, while peripheral nerve stimulation has
recently been used to examine aspects of intermuscular synergist inhibition.
As discussed in this chapter, different lines of evidence exist
to demonstrate that resistance training can induce substantial
changes in nervous system function. Notably, the adaptive
alteration in neuromuscular function elicited by resistance training seems to occur both in untrained individuals, including frail
elderly individuals and patients, as well as in highly trained
athletes. In all of these wildly differing individuals the traininginduced enhancement in neuromuscular capacity leads to
improved mechanical muscle function, which in turn results in
an improved functional performance in various activities of
daily living.
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
c09.indd 105
2.1.2 EFFECTS OF STRENGTH
TRAINING ON MECHANICAL
MUSCLE FUNCTION
2.1.2.1 Maximal concentric and
eccentric muscle strength
The influence of strength training on the maximal contraction
strength of human muscle in vivo has been extensively investigated for the concentric part of the moment–velocity curve
(Aagaard et al., 1996; Caiozzo, Perrine and Edgerton, 1981;
Colliander and Tesch, 1990; Costill et al., 1979; Coyle et al.,
1981; Lesmes et al., 1978; Moffroid and Whipple, 1970; Seger,
Arvidson and Thorstensson, 1998). Also, data exist for the
training-induced change in maximal eccentric muscle strength
(Aagaard et al., 1996; Colliander and Tesch, 1990; Higbie
et al., 1996; Hortobagyi et al., 1996a, 1996b; Komi and Buskirk,
1972; Narici et al., 1989; Seger, Arvidson and Thorstensson,
1998; Spurway et al., 2000).
Following strength training using concentric muscle contractions alone, maximal muscle strength and power were
reported to increase at the specific velocity employed during
training (Aagaard et al., 1994; Caiozzo, Perrine and Edgerton,
1981; Kanehisa and Miyashita, 1983; Kaneko et al., 1983;
Moffroid and Whipple, 1970; Tabata et al., 1990). These and
similar observations have been taken to indicate a specificity of
training velocity and training load. However, it is questionable
whether a generalized concept of training specificity should
exist, since maximal muscle strength and power may also
increase at velocities lower than the actual velocity of training
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
10/21/2010 3:16:33 PM
PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
Moment of Force (Nm)
Based on peak Moment
500
highly strength trained
athlete (Alpine Skiier)
A
sedentary subject
of similar age and
body mass
400
300
200
100
concentric
eccentric
0
-240
-30 0
30
300
200
**
*
*
(Costill et al., 1979; Coyle et al., 1981; Housh and Housh,
1993; Lesmes et al., 1978) as well as at higher velocity (Aagaard
et al., 1994; Colliander and Tesch, 1990; Housh and Housh,
1993). These conflicting findings are likely caused by a variable
involvement of learning effects (Rutherford and Jones, 1986).
Thus, using different training and/or data-recording devices
tends to reduce the influence of learning and hence may provide
a more valid measure of the adaptation in neuromuscular function elicited by strength training.
Untrained individuals typically demonstrate a levelling-off
(plateauing) in maximal muscle strength during slow concentric
muscle contraction, whereas strength-trained individuals do not
(Figure 2.1.1). Notably, the plateauing in maximal muscle
strength can be removed by heavy-resistance strength training
(Aagaard et al., 1996; Caiozzo, Perrine and Edgerton, 1981)
(Figure 2.1.2). Strength training with low external loads and
high contraction speeds appears to have no effect on the plateauing phenomenon (Figure 2.1.2), suggesting that heavy
muscle loadings (>80% 1RM) should be used to diminish or
fully remove the influence of this force-inhibiting mechanism.
Heavy-resistance strength training (loads >85% 1RM)
appears to evoke significant gains in maximal eccentric muscle
strength (Aagaard et al., 1996, 2000a; Andersen et al., 2005;
Colliander and Tesch, 1990; Duncan et al., 1989; Higbie et al.,
1996; Hortobagyi et al., 1996a, 1996b; Komi and Buskirk,
1972; Narici et al., 1989; Seger, Arvidson and Thorstensson,
1998; Spurway et al., 2000,). Moreover, strength training using
maximal eccentric muscle contractions or coupled concentric–
eccentric contractions leads to greater gains in maximal eccentric muscle strength than concentric training alone (Colliander
and Tesch, 1990; Duncan et al., 1989; Higbie et al., 1996
Hortobagyi et al., 1996a, 1996b; Norrbrand et al., 2008). On
the other hand, maximal eccentric muscle strength seems to
remain unaffected by low-resistance strength training (Aagaard
et al., 1996; Duncan et al., 1989; Holm et al., 2008; Takarada
*
Heavy-resistance
strength training
(8 RM loads)
peak
100
eccentric
0
-240
50°
velocity of training
concentric
240
120
30
-120
-30
knee angular velocity (°s-1)
B
Low-resistance
strength training
(24 RM loads)
400
Moment of Force (Nm)
Figure 2.1.1 Maximal concentric, eccentric, and isometric muscle
strength obtained by use of isokinetic dynamometry (KinCom) for the
quadriceps muscle in a highly trained strength athlete (male National
Team Alpine skier) and in a young untrained individual matched for
age and body mass. Notice the marked difference in maximal eccentric
muscle strength between the trained and the untrained subject
**
*
**
240
Angular velocity (°/sec)
c09.indd 106
400
*
SECTION 2
Moment of Force (Nm)
106
300
peak
200
50°
100
velocity of training
eccentric
0
-240
concentric
120
30
-120
-30
knee angular velocity (°s-1)
240
Figure 2.1.2 Maximal concentric and eccentric muscle strength
(quadriceps femoris muscle) measured by isokinetic dynamometry
(KinCom) before (full lines, closed symbols) and after (broken lines,
open symbols) 12 weeks of heavy-resistance (a) or low-resistance (b)
strength training in a group of elite soccer players. Peak moment
(triangles) and isoangular moment (at 50 °; 0 ° = full knee extension)
were obtained, and the velocity used during training is also depicted.
All training was performed using a hydraulic leg extension device
(Hydra fitness). Post > pre: * P < 0.05, ** P < 0.01. Data from
Aagaard et al. (1996)
et al., 2000) (Figure 2.1.2b), suggesting that the involvement of
very high muscle forces during training is probably a key stimulus of adaptive changes in maximal eccentric muscle strength.
2.1.2.2 Muscle power
Maximal muscle strength is typically increased by 20–40% in
response to heavy-resistance strength training of medium to
moderate duration (8–16 weeks) (Aagaard et al., 1996;
Colliander and Tesch, 1990; Häkkinen et al., 1998b). Slightly
greater gains in maximal contractile muscle power of 20–50%
have been observed when heavy-resistance strength training
was performed in young untrained persons, elite soccer players,
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CHAPTER 2.1
1200
Ppeak HRgroup
*
*
*
*
800
*
Heavy load
training (8RM)
400
800
Low load (24RM),
high speed training
400
0
0
0
1200
100
200
300
400
0
500
1200
Ppeak FUgroup
800
*
400
Low load (16 RM)
functional training
POWER (W)
POWER (W)
107
Ppeak HRgroup
*
POWER (W)
POWER (W)
1200
NEURAL ADAPTATIONS TO RESISTANCE EXERCISE
100
200
300
400
500
Ppeak COgroup
800
400
Controls
0
0
0
100
200
300
400
500
–1
VELOCITY (° s )
0
100
200
300
400
500
–1
VELOCITY (° s )
Figure 2.1.3 Peak muscle power (quadriceps femoris muscle) measured by non-isokinetic dynamometry (Hill’s flywheel) before (full lines,
closed symbols) and after (broken lines, open symbols) 12 weeks of heavy-resistance (HR group), low-resistance (LR group), or functionalresistance (FU group; loaded kicking movements) strength training in elite soccer players. A group of non-training controls was also tested (CO
group). Post > pre: * P < 0.05, ** P < 0.01. Data adapted from Aagaard et al. (1994)
and ageing individuals (Aagaard et al., 1994; Caserotti et al.,
2008; De Vos et al., 2005; Duchateau and Hainaut, 1984;
Kaneko et al., 1983; Toji et al., 1997) (Figure 2.1.3). Some of
these studies employed explosive-type training that involved
maximal intentional acceleration of the external load, which
may constitute a key element for achieving large gains in
maximum muscle power output. Notably, strength training
using heavy-resistance muscle loadings (>80% 1RM) appears
to evoke similar or greater increases in maximum muscle power
compared to low-resistance strength training (Aagaard et al.,
1994; De Vos et al., 2005; Duchateau and Hainaut, 1984)
(Figure 2.1.3).
2.1.2.3 Contractile rate of
force development
Rapid force capacity (‘explosive muscle strength’) can be measured as the maximal contractile rate of force development
(RFD) during maximal voluntary muscle contraction (Aagaard
et al., 2002b; Schmidtbleicher and Buehrle, 1987) (Figure
2.1.4). RFD reflects the ability of the neuromuscular system
to generate very steep increases in muscle force within fractions
of a second at the onset of contraction, which has important
functional significance for the force and power generated during
rapid, forceful movements (Aagaard et al., 2002b; Suetta
et al., 2004). A high RFD is vital not only to the trained athlete
c09.indd 107
but also to the elderly individual who needs to counteract
sudden perturbations in postural balance. As discussed in more
detail below, resistance training leads to parallel increases in
RFD and neuromuscular activity (EMG amplitude, rate of EMG
rise) in the initial phase (0–200 ms) of muscle contraction
(Aagaard et al., 2002b; Del Balso and Cafarelli, 2007;
Schmidtbleicher and Buehrle, 1987; Van Cutsem, Duchateau
and Hainaut, 1998).
2.1.3 EFFECTS OF STRENGTH
TRAINING ON NEURAL FUNCTION
The adaptive plasticity of the neuromuscular system in response
to strength training can be ascribed to changes in a large number
of neural and muscular factors. Thus, it is well documented that
strength training can evoke marked changes in muscle morphology and nervous system function (Aagaard, 2003; Duchateau,
Semmler and Enoka, 2006; Folland and Williams, 2007; Sale,
1992). This section will focus on changes in neural function
induced by strength training, while the adaptation in various
muscular factors is addressed in Chapter 2.2.
In brief, the neural adaptation mechanisms involved with
strength training include changes in spinal motor neuron
recruitment and rate coding (firing frequency), motor neuron
excitability, corticospinal excitability, and coactivation of
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300
200
5000
RFD =
ΔForce /ΔTime
0
1500
3000
uVolts
2000
1000
0
Force
Moment
Nm
100
ΔForce
Force (N)
4000
max Force
uVolts
ΔTime
0
uVolts
0.2
0.4
0.6
0.8
VL EMG
-1500
1200
VM EMG
-1200
1000
RF EMG
-1000
Time (seconds)
-400
0
400 800 1200 1600 2000 2400 2800
Time (milliseconds)
Figure 2.1.4 Rapid muscle strength is measured as the contractile rate of force development (RFD); that is, calculated as the slope of the
force–time curve (left panel) or the moment–time curve (right panel, top graph) during the phase of rising muscle force (0–200 ms). RFD is
strongly influenced by the magnitude of neuromuscular activity in the agonist muscles, typically recorded as surface EMG signals (right panel;
quadriceps muscle; vastus lateralis = VL, vastus medialis = VM, rectus femoris = RF). Data adapted from Aagaard et al. (2002b)
integrated surface
EMG from onset
to +dF/dt of MVC
line fit to integral by
method of least squares
Rectified surface
EMG
MVC torque
onset of electrical point where +dF/dtmax
activity
occurs in MVC torque
recording
Rate of MVC torque development
(N·m·s–1)
~200 ms
700.0
650.0
7
600.0
6
5
550.0
3
4
500.0
2
450.0
1
400.0
0.08
0.09
8
12
13
911
10
r = 0.95
p<0.01
0.10 0.11 0.12 0.13
Rate of activation (mV/s)
0.14
Figure 2.1.5 The magnitude of contractile RFD is strongly influenced by the level of neuromuscular activity in the agonist muscles. When the
slope of the integrated EMG (iEMG) curve is determined (left panel, top graph), a strong linear relationship is found to exist between the rate of
accumulated EMG activity (ΔiEMG/Δt) and the rate of rise in contractile force production (RFD = rate of torque development) (right panel).
Reproduced from Del Balso & Cafarelli. 2007. J. Appl. Physiol. © American Physiological Society
antagonist muscles (Aagaard, 2003; Duchateau, Semmler and
Enoka, 2006; Sale, 1992). A line of experimental evidence
has been provided with the use of EMG recording during in
vivo muscle contraction, although inherent methodological
limitations may exist with the recording of surface EMG.
Measurements of evoked spinal responses (H-reflex, V-wave)
can be used to address the adaptability in spinal circuitry function with strength training. In addition, training-induced changes
c09.indd 108
in transmission efficacy in descending corticospinal pathways
have recently been examined.
2.1.3.1 Maximal EMG amplitude
A widely used assessment tool in the evaluation of neural function with training is the recording of EMG signals during
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NEURAL ADAPTATIONS TO RESISTANCE EXERCISE
2.1.3.2 Contractile RFD: changes in
neural factors with strength training
A strong influence of efferent neuromuscular activity on contractile RFD has been demonstrated in a number of studies
(Figure 2.1.5) and parallel gains in contractile RFD and neuromuscular activity evaluated by surface EMG have been
observed following strength training (Aagaard et al., 2002b;
Barry, Warman and Carson, 2005; Del Balso and Cafarelli,
2007; Häkkinen, Alén and Komi, 1985a; Häkkinen, Komi and
Alén, 1985b; Häkkinen et al., 1998a, 2001; Häkkinen and
Komi, 1986; Schmidtbleicher and Buehrle, 1987; Suetta et al.,
2004; Van Cutsem, Duchateau and Hainaut, 1998) (Figure
2.1.6). However, not just heavy-resistance strength training but
c09.indd 109
109
also maximal ballistic training using lower loads can lead to
increased RFD (Duchateau and Hainaut, 1984; Van Cutsem,
Duchateau and Hainaut, 1998). In their classical study Behm
and Sale (1993) compared dynamic and isometric ballistic training performed with maximal intentional acceleration of the
training load, and observed that RFD increased similarly with
both types of training. This finding suggests that the use of an
intended ballistic effort may be more important for inducing
increases in RFD than the actual type of muscle contraction
performed.
Muscle fibre innervation frequency has a strong positive
influence on RFD, which can be observed in single muscle
fibres (Metzger and Moss, 1990a, 1990b) as well as in human
muscles in vivo (De Haan, 1998; Grimby, Hannerz and Hedman,
1981; Nelson, 1996). Notably, RFD continues to increase at
A
**
3500
3000
2500
Nm / sec
maximal voluntary contraction (Figure 2.1.4) The EMG interference signal obtained by surface electrode recording constitutes a complex outcome of motor unit recruitment and motor
neuron firing frequency (rate coding). In addition, the net EMG
signal amplitude is highly influenced by the specific summation
pattern of the individual motor unit action potentials (MUAPs)
(Day and Hulliger, 2001; Farina, Merletti and Enoka, 2004),
which among other things is affected by the degree of motor
unit synchronization (Keenan et al., 2005).
Increased neuromuscular activity evidenced by elevated
EMG amplitudes has been observed following weeks to months
of strength training, which may reflect an increased efferent
neural drive to the muscle fibres (Aagaard et al., 2000a, 2002a,
2002b; Andersen et al., 2005; Barry, Warman and Carson,
2005; Del Balso and Cafarelli, 2007; Häkkinen, Alén and Komi,
1985a; Häkkinen, Komi and Alén, 1985b; Häkkinen et al.,
1987, 1998a, 1998b, 2000, 2001; Häkkinen and Komi, 1983,
1986; Hortobagyi et al., 1996b, 2000; Moritani and DeVries,
1979; Narici et al., 1989; Petrella et al., 2007; Reeves, Narici
and Maganaris, 2004; Schmidtbleicher and Buehrle, 1987;
Suetta et al., 2004; Van Cutsem, Duchateau and Hainaut, 1998).
However, inherent methodological constraints are involved
with the recording and interpretation of muscle-surface EMG,
since the interference summation pattern of the single MUAPs
is not likely to directly reflect the neuronal output of the active
motor neurons (Day and Hulliger, 2001; Farina, Merletti and
Enoka, 2004; Keenan et al., 2005; Yao, Fuglevand and Enoka,
2000). Consequently, a number of studies have failed to demonstrate increased maximal EMG amplitude during MVC following resistance training (Blazevich et al., 2008; Cannon and
Cafarelli, 1987; Narici et al., 1996; Thorstensson et al., 1976),
which could at least in part also be due to altered skin and
muscle tissue conduction properties (i.e. changes in subcutaneous fat thickness, altered muscle fibre pennation angles). To
some extent, however, it is possible to surpass some of the
inherent methodological limitations associated with the recording of muscle-surface EMG by employing measurements of
evoked spinal motor neuron responses (H-reflex, V-wave),
peripheral nerve stimulation, transcranial magnetic or electrical
stimulation (TMS, TES), or by using intramuscular EMG
recordings.
*
*
*
2000
*
1500
1000
500
0
peak
B
30 ms
50
100
450
200 ms
**
400
*
350
300
uVolt
CHAPTER 2.1
250
200
150
VM
VL
*
**
RF
**
**
100
50
0
integrated for
30 ms
50 ms
100 ms
Pre to post training differences: * p < 0.05, ** p < 0.01
Figure 2.1.6 Contractile RFD (a) and neuromuscular activity
(EMG amplitude) (b) obtained before (open bars) and after (hatched
bars) 14 weeks of periodized heavy-resistance strength training.
Open bars = before training, hatched bars = after training. Post > pre:
* P < 0.05, ** P < 0.01. Note the gain in RFD following training,
which was accompanied by marked increases in neuromuscular
activity. Data adapted from Aagaard et al. (2002b)
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Stim rate
400 Hz
200 Hz
120 Hz
80 Hz
Muscle
Force
10 N
0
50
100
150
Time (ms)
200
Figure 2.1.7 Influence of muscle fibre innervation frequency on
contractile RFD. The graph shows the development in isometric
muscle force when using electrical stimulation of the nerve
innervating the rat medial gastrocnemius muscle at various
stimulation frequencies (80, 120, 200, and 400 Hz). The 200 Hz
innervation frequency was sufficient to elicit full tetanic fusion and
maximal muscle force production, whereas a greater RFD was
achieved in the phase of rising muscle force by using 400 Hz
innervation frequency. Data from De Haan (1998)
innervation rates that are higher than full tetanic fusion rate (De
Haan, 1998; Grimby, Hannerz and Hedman, 1981; Nelson,
1996) (Figure 2.1.7). Consequently, the occurrence of very high
(i.e. supramaximal) motor neuron firing frequency at the onset
of rapid muscle force production (Van Cutsem, Duchateau and
Hainaut, 1998) likely plays a functional role to increase maximal
RFD rather than increasing maximal contraction force per se,
in order to increase the level of contractile force exertion in the
initial phase of contraction (0–200 ms).
Strength training can lead to elevated motor neuron firing
frequency during maximal voluntary contraction. For instance,
Van Cutsem, Duchateau and Hainaut (1998) observed a marked
rise in the maximal firing rate of motor neurons innervating
the tibialis muscle at the onset of maximal, forceful contraction
following 12 weeks of ballistic-type resistance training (Figure
2.1.8). Importantly, maximal motor neuron firing frequency
has been reported to increase in both young and elderly individuals following resistance training (Kamen and Knight, 2004;
Van Cutsem, Duchateau and Hainaut, 1998). Untrained elderly
demonstrate lower maximal motor neuron firing rates than
young subjects (Kamen and Knight, 2004; Klass, Baudry and
Duchateau, 2008; Patten, Kamen and Rowland, 2001), but no
age-related differences could be detected following a period
of strength training (Kamen and Knight, 2004; Patten, Kamen
and Rowland, 2001). In other words, the training-induced
increase in maximal motor neuron firing frequency is effective
in overruling the age-related decline in maximal motor unit
discharge rate.
A sixfold elevated incidence of discharge doublet firing was
noticed in the firing pattern of single motor units following
ballistic-type resistance training (pre: 5.2%, post: 32.7% of all
motor units) (Van Cutsem, Duchateau and Hainaut, 1998)
(Figure 2.1.9). This adaptive change in motor neuron firing
c09.indd 110
pattern takes advantage of the catch-like property of skeletal
muscle. Specifically, the presence of discharge doublet firing
with inter-spike intervals <5–10 ms (firing frequency > 100–
200 Hz) is known to result in a marked increase in contractile
force and RFD at the onset of contraction (Binder-MacLeod and
Kesar, 2005; Burke, Rundomin and Zajack, 1976; Moritani and
Yoshitake, 1998) (Figure 2.1.9).
Recurrent Renshaw inhibition of spinal motor neurons has
been considered as a limiting factor for the maximal discharge
rate, and is thought to have a regulating influence on the reciprocal Ia-inhibitory pathway (Hultborn and Pierrot-Deseilligny,
1979). Animal experiments show that Renshaw cells receive
several types of supraspinal synaptic input that can enhance as
well as depress the recurrent pathway (Hultborn, Lindström
and Wigström, 1979; Pierrot-Deseilligny and Morin, 1980).
Compared with tonic steady-force contractions, Renshaw cell
activity is more inhibited during maximal phasic muscle contractions, resulting in reduced recurrent inhibition in the latter
condition (Pierrot-Deseilligny and Morin, 1980). Consequently,
the use of explosive-type resistance training (i.e. contractions
involving high RFD) may be optimal for evoking changes in
the maximum firing rate of spinal motor neurons. This effect
may be restricted to large proximal muscle groups, since recurrent inhibition appears to be absent in the smaller distal muscles
of the hands and feet.
Resistance training can lead to tendon hypertrophy and
increased muscle tendon stiffness (Arampatzis, Karamanidis
and Albracht, 2007; Kongsgaard et al., 2007). The traininginduced increase in tendon stiffness is likely to also contribute
to the observed rise in RFD, since contractile RFD is positively
affected by the stiffness of the series-elastic force-transmitting
structures (Bojsen-Møller et al., 2005; Wilkie, 1950).
There are several important functional consequences of
increasing RFD by means of strength training; the traininginduced rise in RFD allows for an enhanced acceleration of
movement, elevated limb speed during short-lasting movements, and increased muscle force and power during fast movements. Notably, the training-induced rise in contractile RFD is
not only important to the athlete but also for elderly individuals
when walking at high horizontal speed (crossing a busy street,
for example) (Suetta et al., 2004) and to ensure an optimal
postural balance (Izquierdo et al., 1999b).
2.1.3.3 Maximal eccentric muscle
contraction: changes in neural factors
with strength training
Eccentric muscle contractions involve exertion of muscle fibre
force during simultaneous muscle lengthening. For untrained
individuals, the shape of the contractile force–velocity relationship in vivo deviates markedly during maximal eccentric contraction from that obtained in isolated muscle (Figure 2.1.10).
In contrast, strength-trained individuals appear to be able to
produce very high levels of maximal eccentric muscle force
compared to untrained subjects (see Figure 2.1.1). High levels
10/18/2010 5:11:29 PM
A
10 N m
b
** *
b
*
* ***
50 ms
c
*
*
*
*
c
*
*
0.5 ms
*
*
1mV
10 ms
pre training
post training
B
Motor Unit
firing rate (Hz)
200
*Post > Pre, P < 0.001
200
*
150
*
150
*
100
100
50
50
0
I. II. III.
I. II. III.
Interspike intervals
0
Figure 2.1.8 (a) Motor unit firing patterns recorded in the ankle dorsiflexor muscles (TA) during maximal ballistic dynamic contractions (40%
MVC load) before (left-side graphs) and after (right-side graphs) 12 weeks of ballistic-type strength training. Note that shorter inter-spike
intervals and a higher sustained firing rate were observed following training. From Van Cutsem, Duchateau and Hainaut (1998). (b) Motor unit
firing rates measured at the onset of contraction before (open bars) and after (hatched bars) ballistic-type strength training. Note the marked
increase (∼100%) in motor unit firing frequency. Data reported by Van Cutsem, Duchateau and Hainaut (1998)
pre training
post training
A
*
40
Post > Pre
(P < 0.001)
40
30
Catchlike-inducing stim train:
initial doublet (5 ms) + 12 Hz stim
B
30
Constant-frequency Train
Catchlike-inducing Train
600
500
20
20
10
10
Force (N)
Incidence of
discharge doublets (%)
*
400
300
Constant freq train:
12 Hz stim
200
100
0
0
pre
post
training
0
0
200
400
600
800
1000 1200 1400
Time (ms)
Figure 2.1.9 (a) The incidence of motor unit doublet firings observed in the ankle dorsiflexors (TA muscle) before (open bar) and after
(hatched bar) 12 weeks of ballistic-type strength training. Note that doublet firing was sixfold elevated after the period of training. Data reported
by Van Cutsem, Duchateau and Hainaut (1998). (b) Effect of doublet firing on contractile RFD (quadriceps femoris muscle). Addition of an
initial doublet (5 ms inter-spike interval) to an innervation pattern of constant frequency stimulation (12 Hz) results in a highly elevated RFD
during the initial phase of rising muscle force. A similar albeit less marked trend can be observed during tetanic stimulation. Reproduced from
Binder-Macleod & Kesar. 2005
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PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
of eccentric muscle strength are required in many types of
sports and exercise, as this provides an enhanced capacity to
decelerate movements in very short time and thereby perform
fast stretch–shortening cycle (SSC) actions (e.g. rapid jumping),
while also allowing rapid shifts in movement direction (e.g. fast
side-cutting movements). Further, high eccentric strength in
antagonist muscles provides enhanced capacity to decelerate
and halt movements at the end-ROM to protect ligaments (e.g.
ACL) and joint capsule structures (Aagaard et al., 1998). High
levels of eccentric antagonist muscle strength also allow a more
rapid limb deceleration during fast ballistic movements, which
yields more time for limb acceleration and hence allows a
higher movement speed to be reached (Jaric et al., 1995).
It has been suggested that a neural regulatory mechanism
that limits the recruitment and/or discharge rate of motor units
exists during maximal voluntary eccentric muscle contraction
(Aagaard et al., 2000a). In support of this notion, the neuromuscular activity (EMG amplitude) recorded during maximal
eccentric contractions appears to be markedly reduced compared to concentric contractions (Aagaard et al., 2000a;
Amiridis et al., 1996; Andersen et al., 2005; Duclay and Martin,
2005; Duclay et al., 2008; Kellis and Baltzopoulos, 1998; Komi
et al., 2000; Westing, Cresswell and Thorstensson, 1991)
(Figure 2.1.11). Superimposed muscle-twitch recordings have
indicated that central activation is substantially reduced during
maximal eccentric muscle contraction in untrained individuals
(Babault et al., 2001; Webber and Kriellaars, 1997). In further
support of an inhibitory mechanism, reduced evoked spinal
motor neuron responses (H-reflex amplitude; see Section
2.1.3.4) have been observed during maximal eccentric muscle
Contractile muscle force
140
120
100 = maximal isometric force
80
60
40
20
eccentric
concentric
muscle lengthening
muscle shortening
-60
-40
-20
0
20
40
60
80
Muscle contraction velocity
100
percent
Figure 2.1.10 The force–velocity relationship obtained for isolated
muscle when activated by electrical stimulation (full line; Edman,
1988; Hill, 1938; Katz, 1939) and when measured in vivo during
maximal voluntary contraction efforts in physically fit human subjects
using isokinetic dynamometry (triangles, broken line; Westing, Seger
and Thorstensson, 1990). Positive velocities denote muscle shortening
(concentric contraction), negative velocities denote muscle
lengthening (eccentric contractions), and zero velocity denotes
isometric muscle contraction. All force values are expressed relative
to maximal isometric force. Note that during eccentric muscle
contraction there is a marked deviation between in vivo and in vitro
muscle force capacity
700
Force and aEMG at 110° elbow angle
(N)
ECC
CONC (mV)
ISOM
1.2
600
Angle
Force
Preactivation
(1s)
BB
500
55°
400
110°
165°
BR
300
1
0.8
0.6
FORCE
200
100
0
1.4
0.4
TB
–4 –3 –2 –1 0
1
2
3
0.2
0
4 rad∗s–1
Figure 5—Force and aEMG of biceps brachii
(BB), brachioradialis (BR) and triceps brachii
(TB) with different movement velocities in
eccentric, isometric and concentric action at
elbow angle 110°.
Figure 2.1.11 Right panel: maximal voluntary muscle strength (diamond symbols, left vertical axis) and neuromuscular activity (EMG
amplitude, right vertical axis) for the elbow flexors (BB = biceps brachii, BR = brachioradialis) and the antagonist elbow extensors (TB = triceps
brachii) during concentric (positive velocities), isometric (zero velocity), and eccentric (negative velocities) contraction performed in an
isokinetic dynamometer. Left panel: example of data recording during eccentric muscle contraction. Data from Komi et al. (2000)
c09.indd 112
10/18/2010 5:11:29 PM
Isometric
Concentric
Hmax
1 mV
Mhmax
Eccentric
Hmax
Mhmax
NEURAL ADAPTATIONS TO RESISTANCE EXERCISE
Mhmax
Hmax
A
Percent
CHAPTER 2.1
200
*
*
180
*
*
Quadriceps
force moment
(percent)
*
160
113
*
140
120
100
Mmax
100
Mmax
Percent
Mmax
1 mV
90
*
*
*
mean EMG
Quadriceps
(percent)
80
70
60
-240 eccentric
10 ms
contraction in untrained individuals (Duclay et al., 2008)
(Figure 2.1.12).
Importantly, the apparent suppression in motor neuron activation during maximal eccentric contraction can be downregulated or removed by use of heavy-resistance strength training.
Thus, the observed suppression in EMG amplitude during
maximal eccentric contraction is partially abolished in parallel
with a gain in maximal eccentric muscle strength after periods
of heavy-resistance strength training, in turn resulting in a
marked increase in maximal eccentric muscle strength (Aagaard
et al., 2000a; Andersen et al., 2005) (Figure 2.1.13a). The gain
in maximal eccentric muscle strength induced by heavyresistance strength appears to be strongly associated with the
corresponding increase in neuromuscular activity, indicating
the pivotal importance of neural adaptation in allowing this
change to occur (Figure 2.1.13b).
The specific neural pathways responsible for the suppression
in neuromuscular activity during maximal eccentric contraction
remain unidentified. During maximal voluntary muscle contraction, efferent motor-neuronal output is influenced by central
descending pathways, afferent inflow from group Ib Golgi
organ afferents, group Ia and II muscle spindle afferents, group
III muscle afferents, and by recurrent Renshaw inhibition. All
of these pathways may exhibit adaptive plasticity with training.
c09.indd 113
B 120
Δ% ECC Torque at 30°/s
Figure 2.1.12 H-reflex responses recorded in the soleus muscle
during isometric, concentric, and eccentric plantarflexor contractions
of maximal voluntary effort (top panel). Note the depression in
H-reflex amplitude during maximal eccentric contraction, suggesting
reduced spinal motor neuron excitability and/or increased presynaptic
or postsynaptic inhibition. The finding that maximal M-wave (Mmax)
remained unchanged across contraction modes (bottom panel)
verifies that the depressed H-reflex response during eccentric
contraction was not a recording artefact. Data from Duclay et al.
(2008)
-30
30 concentric
240
Knee angular velocity (°s-1)
r = 0.89, p<0.001
100
80
60
40
20
0
0
20
40
60
80 100 120 140
Δ% ECC norm EMG at 30°/s
Figure 2.1.13 (a) Maximal contraction strength and neuromuscular
activity during maximal eccentric (negative velocities) and concentric
(positive velocities) muscle contractions before (solid lines) and after
(broken lines) 14 weeks of strength training. All values are
normalized relative to fast concentric contraction. Notice that the
suppression in neuromuscular activity during eccentric and slow
concentric contraction prior to training was reduced following
training. Data from Aagaard et al. (2000a). (b) The training-induced
gain in maximal eccentric muscle strength is strongly related to the
corresponding rise in neuromuscular activity. Data from Andersen
et al. (2005)
Interestingly, recent experiments showed that evoked spinal
V-wave responses (see Section 2.1.3.4) increased during
maximal eccentric plantarflexor contraction following heavyresistance (maximal eccentric) strength training (Duclay et al.,
2008), indicating that supraspinal and/or spinal neuronal
pathways were altered with resistance training. One likely
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mechanism for the marked increase in eccentric muscle strength
with resistance training could be a downregulation in spinal
inhibitory interneuron activity mediated via Golgi organ Ib
afferents. Furthermore, the H-reflex response appears to be
markedly suppressed during both active and passive muscle
lengthening compared to shortening (Duclay et al., 2008;
Pinniger et al., 2000) (see Figure 2.1.12), suggesting the presence of presynaptic inhibition of Ia afferents during eccentric
muscle contraction. A training-induced reduction in presynaptic
inhibition of Ia afferents would therefore result in an elevated
excitatory inflow to the spinal motor neuron pool during
maximal eccentric muscle contraction, which would increase
maximal eccentric muscle strength.
Important functional consequences emerge when maximal
eccentric muscle strength is increased by means of resistance
training. Thus, elevated eccentric muscle strength enables
more rapid performance of deceleration and SSC movements,
side-cutting, and jumping actions. Furthermore, traininginduced gains in eccentric antagonist muscle are important to
ligament (ACL) and joint protection during sports and exercise.
Elevated maximal eccentric muscle strength also allows elderly
individuals to perform daily events such as stair descent in a
safer manner.
Motor cortex
EMG
amplifier
Stimulator
Sensory Ia
afferent axone
Spinal cord
Muscle
a-motoneuron
axone
Mmax
V
2 mV
10 ms
2.1.3.4 Evoked spinal motor
neuron responses
The Hoffman (H) reflex can be used to examine traininginduced changes in spinal circuitry function at rest and during
active contraction, as the size of the evoked H-reflex amplitude
reflects the level of spinal motor neuron excitability and the
magnitude of presynaptic inhibition of muscle-spindle Ia afferents (Nielsen and Kagamihara, 1992; Schieppati, 1987). The
V-wave is a variant of the H-reflex that can be elicited when
supramaximal stimulation of the peripheral nerve is superimposed on to voluntary muscle contraction (Aagaard et al.,
2002a; Hultborn and Pierrot-Deseilligny, 1979; Upton,
McComas and Sica, 1971) (Figure 2.1.14). When obtained
during maximal muscle contraction, the alteration in H-reflex
and V-wave amplitude may be used to quantify the traininginduced rise in efferent output from spinal motor neurons (Vwave) and motor neuron excitability and/or presynaptic
inhibition (H-reflex, V-wave) (Aagaard et al., 2002a; Del Balso
and Cafarelli, 2007; Sale et al., 1983). Importantly, the evoked
motor neuron responses (peak-to-peak amplitude or area) are
normalized to the maximal M-wave amplitude in order to eliminate or diminish the measuring bias normally associated with
repeated surface EMG recording.
Elevated V-wave and H-reflex amplitudes have been
observed during maximal muscle contraction following months
of resistance training (Aagaard et al., 2002a; Duclay et al.,
2008; Sale et al., 1983) (Figure 2.1.15). A rise in V-wave
amplitude also was found after short-term (3–4 weeks) strength
training (Del Balso and Cafarelli, 2007; Fimland et al., 2009a,
2009b, 2010), as well as following eccentric strength training
(Duclay et al., 2008). While the peak-to-peak amplitude of the
c09.indd 114
Figure 2.1.14 V-wave responses recorded in the soleus muscle by
electrical stimulation of Ia afferent axons in the peripheral nerve (n.
tibialis) during maximal voluntary muscle contraction. The peak-topeak amplitude of the V-wave reflects the magnitude of central
descending motor drive as well as the excitability state of spinal
motor neurones, including presynaptic inhibition of Ia afferent
synapses and postsynaptic inhibition. Adapted from Aagaard,
2002a
H-reflex recorded during MVC increased following 14 weeks
of dynamic strength training (Aagaard et al., 2002a), elevated
H-reflex responses were recorded at submaximal force levels
after shorter periods (3–5 weeks) of strength training
(Holtermann et al., 2007; Lagerquist, Zehr and Docherty,
2006). Altogether these findings suggest that the neural adaptation to strength training can be elicited within a relatively short
time frame of training, and additionally that neural adaptation
may take place throughout the continued time course of training
(see Figure 2.1.16).
When post-training V-waves were recorded at muscle force
levels corresponding to pre-level MVC, no change in the
evoked V-wave response could be detected, whereas a rise in
V-wave amplitude was found at post-training MVC (Del Balso
and Cafarelli, 2007) (Figure 2.1.16). This finding clearly illustrates and underlines that a close cause–response relationship
exists between the change in efferent motor neuron output
and the gain in maximal muscle force induced by resistance
training.
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CHAPTER 2.1
175
150
**
125
100
0.4
75
50
0.2
Moment of force (Nm)
*
*
0.6
115
200
*
pre training
post training
0.8
Peak-to-Peak Amplitude
( normalized to Mmax)
NEURAL ADAPTATIONS TO RESISTANCE EXERCISE
25
0.0
0
V-wave
CONC
H-reflex
ECC
Plantar flexor strength
Figure 2.1.15 Changes in spinal evoked H-reflex and W-wave responses, and and in maximal muscle strength elicited by 14 weeks of strength
training. Enhanced H-reflex and V-wave responses were observed following the period of training, indicating that neural adaptive changes
occurred at both spinal and supraspinal levels. Pre > post: * P < 0.05, ** P < 0.01. Adapted from Aagaard, 2002a
0.30
1.0
0.25
*
§
*
0.6
0.20
*
§
0.4
*
0.2
Pre
Post
*
Pre-test
Day 7
Post-test-V1
Post-test-V2
*
V / Mmax
V/Mmax
0.8
*#
0.15
§
0.10
0.0
50
75
100
Contraction intensity (% MVC)
Figure 2.1.16 Evoked spinal V-wave responses recorded in the
soleus muscle during isometric plantarflexions at 50, 75, and 100%
MVC. * Greater than pre-test (P < 0.05). Post-test V2: V-wave
response recorded post-training at pre-MVC. Reproduced from Del
Balso & Cafarelli. 2007. J. Appl. Physiol. © American Physiological
Society
Recent data have shown that strength training can lead to
enhanced spinal circuitry function in patients with neuropathy
such as multiple sclerosis (MS) (Fimland et al., 2010). MS is a
neuro-degenerative disease affecting the nervous system,
leading to loss of myelinization and destruction of peripheral
axons, and consequently MS patients demonstrate 30–70%
reduced muscle strength compared to healthy control subjects
(Ng et al., 2004; Rice et al., 1992). Elevated V-wave responses
and increased MVC were recently observed in middle-aged MS
patients following 15 sessions of heavy-resistance strength
c09.indd 115
0.05
0.00
Strength training group
(n=7)
Control group
(n=7)
Figure 2.1.17 Evoked spinal V-wave responses recorded in the
soleus muscle during maximal isometric plantarflexion in multiple
sclerosis patients before (black bars) and after (grey bars) four weeks
of heavy-resistance strength training. Pre > post: * P < 0.05, #
different from controls P < 0.05. Reproduced from Fimland. 2010,
Eur. J. App. Physiol. © American Physiological Society
training, suggesting that strength training may provide an effective tool for preventing or retarding the gradual decline in motor
function typically seen with this condition (Figure 2.1.17).
The training-induced rise in V-wave and H-reflex amplitude
indicates the presence of enhanced neural drive in descending
corticospinal pathways, elevated motor neuron excitability,
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PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
reduced presynaptic inhibition of Ia afferents, and/or reduced
postsynaptic motor neuron inhibition (Aagaard, 2003). When
obtained in resting conditions, however, the H-reflex response
appear to remain unaltered by resistance training (Aagaard
et al., 2002a; Del Balso and Cafarelli, 2007; Duclay et al., 2008;
Scaglioni et al., 2002), suggesting that the training induced
change in spinal circuitry function does not involve chronic
changes in neuroanatomy (e.g. increased number of Ia afferent
terminals, etc.), since these would be expected to cause changes
in resting H-reflex amplitude.
2.1.3.5 Excitability in descending
corticospinal pathways
In recent years TMS and TES have been increasingly used to
assess training-induced changes in the transmission efficacy in
descending motor pathways from the cerebral cortex to the
muscle fibres, including the spinal cord. Via analysis of the
evoked EMG responses recorded in the target muscle (so-called
motor-evoked potentials, MEPs) (Figure 2.1.18), information
can be obtained about the level of corticospinal excitability,
cortical recruitment threshold, recruitment gain, as well as intracortical inhibition and facilitation.
Somewhat equivocal results have been obtained with these
newly-developed techniques. MEPmax and the input–output
slope obtained by TMS in the biceps brachii muscle during
low-level contraction (5% of max EMG) remained unchanged
following short-term (4 weeks) strength training (for definition
of TMS parameters see Figure 2.1.18b), whereas marked
increases were found in isometric and dynamic MVC (Jensen,
Marstrand and Nielsen, 2005). In a more recent study, however,
maximal MEP amplitude evoked by TMS during low-force
tonic contraction (10% MVC) increased by 32% in response
to four weeks of isometric strength training of the ankle dorsiflexors (TA muscle), suggesting that the period of strength
training led to an increased excitability in descending corticospinal pathways (Griffin and Cafarelli, 2007). In addition, taskand training-specific enhancements in MEP size and MEP
recruitment were recently reported following four weeks of
ballistic-type strength training for the ankle dorsiflexors and
plantarflexors (Beck et al., 2007). MEP recruitment evaluates
the input–output properties of the motor system, including
excitatory synaptic transmission efficacy in the motor cortex
and density of corticospinal projections to the contracting
muscles. The authors concluded that supraspinal sites were
involved in the adaptation to ballistic (‘explosive-type’)
strength training, and that such training is capable of altering
corticospinal facilitation, possibly by changing recruitment gain
(Beck et al., 2007).
In contrast, strength training has also been reported to
decrease MEPmax and the slope of the input–output relation
at rest (Lundbye Jensen, Marstrand and Nielsen, 2005), and
to result in a reduced ratio between evoked MEP size and
muscle torque production or level of background EMG during
tonic contraction of moderate intensity (40–60% of MVC),
with no changes observed at lower contraction intensities
c09.indd 116
(Carroll, Riek and Carson, 2002). Similar findings emerged
for TES-induced MEPs (Carroll, Riek and Carson, 2002). TES
(transcranial electrical stimulation) recruits corticospinal neurones directly by electrical depolarization of their axones at
deeper sites in the brain, whereas TMS (transcranial magnetic
stimulation) recruits corticospinal cells via lateral transsynaptic
excitation in the cortical layer. The TES-induced MEP response
is therefore much less influenced by the excitability state of
the motor cortex than that produced using TMS, and the
above findings of similar changes in TMS- and TES-evoked
MEP properties consequently led to the suggestion that subcortical rather than cortical sites might be responsible for the
adaptive plasticity with strength training (Carroll, Riek and
Carson, 2002).
These contradictory findings, manifested by enhanced
versus reduced MEPs respectively, on the influence of strength
training on cerebral motor cortex function may be related to the
different muscles examined (i.e. hand versus lower leg), differences in the motor tasks used during training and testing including differences in contraction intensity, and possibly the specific
TMS/TES-stimulation paradigm used.
2.1.3.6 Antagonist muscle coactivation
Coactivation of antagonist muscles is an inherent element in
normal human movement (Aagaard et al., 2000b; DeLuca and
Mambrito, 1987; Smith, 1981). The presence of antagonistmuscle coactivation protects ligaments from excessive strain at
the end-range of joint motion (Draganich and Vahey, 1990;
More et al., 1993), ensures a homogenous distribution of compression forces over the articular surfaces of the joint (Baratta
et al., 1988), and results in increased joint and limb stiffness
(Milner and Cloutier, 1993). In addition, an adequately high
level of antagonist muscle strength is important for the execution of fast, ballistic limb movements. Thus, high eccentric
antagonist strength allows for a shortened phase of limb deceleration at the end of movement, thereby increasing the time
available for limb acceleration, resulting in an increased
maximal movement velocity (Jaric et al., 1995). Elevated
agonist–antagonist muscle coactivation is typically observed
during unstable motor tasks or during the anticipation of compensatory muscle forces (DeLuca and Mambrito, 1987).
Increased antagonist muscle coactivation can be observed in
elderly individuals during stair walking (Hortobagyi and
DeVita, 2000; Larsen et al., 2008), and elevated levels of
antagonist muscle coactivation have been implicated as a risk
factor for exercise-induced rib stress fracture in elite rowers
(Vinther et al., 2006). Conversely, a rise in hamstring antagonist coactivation during active knee extension results in reduced
strain and stress forces in the anterior cruciate ligament (ACL),
potentially protecting against ACL injury (Aagaard et al.,
2000b; Draganich and Vahey, 1990; More et al., 1993).
Increasing attention has been directed to the aspect of medial
versus lateral antagonist muscle coactivation, since female elite
soccer players with reduced medial hamstring muscle coactivation during rapid, forceful side-cutting manoeuvres were more
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NEURAL ADAPTATIONS TO RESISTANCE EXERCISE
117
A
(i)
Rest
(ii)
TMS
Tonic contraction
Intensity of stimulation
25%
30%
35%
40%
45%
50%
55%
Corticomotoneuronal
cells
60%
65%
70%
75%
1 mV
20 ms
80%
m.biceps brachii
EMG
m.triceps brachii
EMG
MEP amplitude (% of Mmax)
(iii)
Motoneurones
Rest
40
Tonic contraction
30
20
10
0
20
40
60
80 20
40
60
80
Intensity of stimulation
(% of maximal stimulator output)
B
MEP Size (% Mmax)
40
tangent at peak slope
MEPmax
30
20
½MEPmax
10
0
10
X intercept of tangent
35
S50
60
85
110
Figure 2.1.18 (a) Transcranical magnetic stimulation (TMS) (i) gives rise to evoked motor potential (MEP) in the muscle (ii), where steeper
input–output relationships are observed during active muscle contraction compared to rest (iii). From Jensen, Marstrand and Nielsen (2005). (b)
Analysed features of the MEP input–output relationship. Reproduced from Carroll, 2002. J. Physiol. © John Wiley & Sons, Ltd.
c09.indd 117
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PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
likely to sustain serious ACL injury compared to players demonstrating a more uniform medial-to-lateral coactivation pattern
(Zebis et al., 2009).
It remains to be settled whether strength training per se
leads to altered patterns of antagonist coactivation. Decreased
antagonist coactivation may seem desirable since it leads to
increased net joint moment (agonist muscle moment minus
antagonist muscle moment). On the other hand, a decrease in
antagonist muscle coactivation might lead to a reduced stabilization of the joint, as discussed above. Following strength
training, the magnitude of antagonist muscle coactivation has
been reported to decrease (Carolan and Cafarelli, 1992;
Häkkinen et al., 1998a, 2000, 2001), increase (Baratta et al.,
1988), or remain unchanged (Aagaard et al., 2000b, 2001;
Colson et al., 1999; Häkkinen et al., 1998a, 2000, 2001;
Hortobagyi et al., 1996b; Reeves, Maganaris and Narici, 2005;
Valkeinen et al., 2000). During maximal static knee extension
(isometric quadriceps contraction), older individuals appear to
demonstrate elevated coactivation of the antagonist hamstring
muscles than younger subjects (Häkkinen et al., 1998a, 2000;
Izquierdo et al., 1999a; Macaluso et al., 2002). In elderly individuals, antagonist hamstring coactivation was found to
decrease in response to six months of heavy-resistance strength
training, reaching a level similar to that observed in middleaged subjects (20–25% of maximal agonist activity), which
remained unaltered with training (Häkkinen et al., 1998a,
2000). Antagonist muscle coactivation is markedly elevated
when uncertainty exists in the motor task (DeLuca and
Mambrito, 1987). Consequently, elderly subjects, and to a
lesser extent young individuals, may occasionally demonstrate
very high levels of coactivation (30–45% of maximal agonist
activity) during the initial pre-training assessment of MVC.
This may, at least in part, explain why some studies have
A
Force (N)
SECTION 2
B
50
young
25
1
2
3
Time (s)
4
5
4
5
100
pre
75
50
post
25
0
0
1
2
3
Time (s)
Figure 2.1.19 Force steadiness and force accuracy. Tracking of
25-N target force during 5 sec slow (15 °/s) eccentric quadriceps
contraction (post 10 familiarization trials). (a) Typical force tracings
obtained in old and young subjects demonstrating increased
SD(force) and reduced force accuracy in old versus young
individuals. (b) Reduced SD(force) and improved force accuracy in
old subject after a period of strength training. Reproduced from
Hortobagyi et al., 2001
adaptation
“muscle volume training”
old
75
0
Morphological *
6-12 RM loads
100
0
Force (N)
118
mechanisms
↑ Maximal muscle strength
↑ Explosive muscle strength
(Rate of Force Development)
1-8 RM loads
“explosive type training”
Neural
adaptation
mechanisms **
↑ Eccentric muscle strength
Neural changes to strength training **
↑ neuromuscular activity ( ↑ iEMG )
↑ motorneuron excitability and/or reduced presynaptic inhibition
↓ EMG depression in ECC contraction
Muscular changes to strength training
*
↑ muscle cross-sectional area ( CSA )
↑ CSA, type II muscle fibres ( type II MHC isoforms )
changes in muscle architecture ( fibre pennation )
Figure 2.1.20 Neural and muscular changes to strength training. Graph modified from Aagaard, 2003
c09.indd 118
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CHAPTER 2.1
NEURAL ADAPTATIONS TO RESISTANCE EXERCISE
consistently observed a decrease in antagonist muscle coactivation following strength training when the majority have not
been able to confirm this adaptation.
2.1.3.7 Force steadiness, fine
motor control
The ability for fine motor control can be evaluated by analysis
of the steadiness of constant-force muscle contraction.
Steadiness can be measured as the variance (SD) in the fluctuation in muscle force while a subject tries to sustain a certain
target force (i.e. 10% of max force).
Notably, greater force error and less steady muscle force
production (elevated SD) can be seen during submaximal
constant-force contractions in elderly compared to young subjects (Hortobagyi et al., 2001; Tracy and Enoka, 2002) (Figure
2.1.19). Substantial reductions in force error and force variability (i.e. diminished SD(force)) have been observed following strength training in ageing individuals (Hortobagyi
et al., 2001; Tracy, Byrnes and Enoka, 2004; Tracy and Enoka,
2006) (Figure 2.1.19). These findings demonstrate that strength
c09.indd 119
119
training can lead to improved force steadiness and fine motor
control in the elderly.
2.1.4 CONCLUSION
Different lines of evidence have been presented in this chapter
to demonstrate that strength training elicits a substantial variety
of beneficial alterations in nervous system function. Specifically,
a huge range of training-induced plasticity appears to exist at
spinal, supraspinal, and cortical levels. The neural adaptation to
strength training comprises gains in maximal muscle strength,
rapid force capacity (RFD), and maximal eccentric muscle
strength (Figure 2.1.20). Most importantly, the adaptive
improvement in neuronal function elicited by resistance training can occur both in untrained individuals, including frail
elderly individuals and patients, and in highly trained athletes.
In all individuals the training-induced enhancement in neuromuscular capacity leads to improved mechanical muscle
function, which in turn results in an improved functional performance in various activities of daily living, including sports
and physical exercise.
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2.2 Structural and Molecular
Adaptations to Training
Jesper L. Andersen, Institute of Sports Medicine Copenhagen, Bispebjerg Hospital, Copenhagen, Denmark
2.2.1
INTRODUCTION
There are many reasons for conducting resistance exercise
strength training: improvement of athletic performance, general
health, rehabilitation, counteraction of ageing-induced muscle
atrophy, or the simple pleasure of working the muscles after a
long day at the office (Fry, 2004).
Ultimately strength training is conducted with the purpose
of making muscles stronger. The path to reaching this goal is
bifurcated and can in principle be reached by changes in neuromuscular recruitment pattern or by increasing muscle size. In
practice, it is usually a combination of the two. This chapter
deals with adaptations of the muscle when submitted to strength
training.
Why do muscles grow when subjected to resistance training? Why is growth more pronounced with certain types and
intensities of resistance training? Why does ingestion of relatively small amounts of protein after resistance training facilitate muscle growth? Does human skeletal muscle change fibre
type composition with strength training? What is the role of
satellite cells in muscle hypertrophy? How does concurrent
training influence the adaptations in the muscle? These are all
areas of human skeletal muscle adaptation to strength training
in which development has occurred in recent years. It is emphasized that it is not the ambition of this chapter to delve deeply
into specific areas but rather to put spotlight on selected issues
of current interest. A number of recommendations are provided,
which are principally aimed at athletes, but can with simple
adjustments also be useful for elderly people or in a wide range
of rehabilitation programs.
2.2.2 PROTEIN SYNTHESIS AND
DEGRADATION IN HUMAN
SKELETAL MUSCLE
Passing any gym in which strength training is taking place, the
sight of people moving their protein-shakes along with them as
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
c10.indd 125
they switch from one machine to another is more the rule than
the exception. This phenomenon was not observed 10–15 years
ago. The massage of protein supplementation has certainly
found a foothold in the sporting and training community. But
does it have any significant effect on the development of muscle
mass? To try to answer that question, we have to start out by
looking at the more fundamental mechanisms related to growth
and reduction of skeletal muscle.
The skeletal muscle mass is maintained when there is an
equilibrium between muscle protein synthesis and muscle
protein breakdown. A disturbance of the balance in favour of
one side over the other will lead to either muscle hypertrophy
or muscle atrophy. Since the purpose of strength training is to
increase muscle strength and in most cases to increase muscle
volume, it is obvious that it is unfavourable for muscle protein
degradation to exceed muscle protein synthesis, which eventually leads to muscle atrophy. Nevertheless, this scenario can
occur for instance in an overtraining situation, and will always
occur during detraining or tapering periods. While the first of
these two scenarios is of course very undesirable, the latter is
controlled and calculated, and in most cases the atrophy signals
will not dominate, but will be dampened and insufficiently large
to maintain the hypertrophied state of the well-trained athlete’s
muscles.
To achieve growth of the muscle fibres a positive net protein
balance has to occur; during the post-exercise phase muscle
protein synthesis has to exceed muscle protein breakdown. It
is technically difficult to exactly measure protein breakdown
during resistance training, but the few attempts made suggest
that no major differences from the nontraining situation occur
(Durham et al., 2004; Kumar et al., 2009a; Tipton et al., 2001).
Thus it hasn’t convincingly been established what happens
with muscle protein synthesis during resistance training, but
extracting data from the few human studies conducted and
extrapolating from various animal studies it seems that most
kinds of muscle activity, and especially resistance-related
muscle activity, will decrease protein synthesis during the
actual training phase (Bylund-Fellenius et al., 1984; Dreyer
et al., 2006; Fujita et al., 2009). Therefore a negative net
protein balance during the actual resistance training session
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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seems probable. Nevertheless, the change in protein synthesis
and the breakdown that happens during exercise are relatively
small and occur within a limited timeframe, and are therefore
of less importance than the changes that are manifested in the
hours and days after the training session.
In the initial post-exercise phase muscle protein synthesis is
increased, but so is muscle protein breakdown (Dreyer et al.,
2006; Fujita et al., 2009; Kumar et al., 2009a; Phillips et al.,
1997). The actual curves signifying protein synthesis and
protein breakdown follow specific patterns; one common
feature is that after strenuous resistance training exercise the
protein synthesis is elevated for approximately 48 hours (Kumar
et al., 2009a), and sometimes as much as 72 hours (Miller
et al., 2005), whereas the protein breakdown is back to pretraining levels within 24 hours after exercise (Phillips et al.,
1997). As described later, the post-training protein synthesis in
the first hours after training is greatly influenced by the fed state
of the subject during and immediately after the training bout,
whereas the protein breakdown is much less affected by the
feeding status (Rasmussen and Phillips, 2003). A crude general
rule is that if the subject is in a fed stage during or immediately
after the training session then the protein synthesis in the postexercise phase will at all times exceed the protein breakdown,
while the exact opposite is the case if the subject is in a fasted
state (Kumar et al., 2009a; Phillips et al., 1997).
Providing protein to the system in conjunction with resistance training will at least double the increase in protein synthesis as compared to no protein provided (Kumar et al., 2009a;
Rennie et al., 1982). There is great scientific, as well as commercial, interest in the quality (proportions of different amino
acids and digestibility) of the supplementary protein to be
ingested in connection with resistance exercise, which mean
that much time, effort, and money has been invested in trying
to design the optimum amino acid compound for use in resistance training (Tang and Phillips, 2009). Nevertheless, whether
the protein comes from a regular meal or a protein supplementation product may not have a major influence. The composition
of the amino acids (e.g. if the protein ingested originates from
whey, casein, or soy) will definitely have some modulating
importance (Cuthbertson et al., 2005; Tang and Phillips, 2009;
Tang et al., 2009), but it seem as if the most important factor
is that protein is ingested. Furthermore, there seems to be a
dose–response relation between the amount of protein provided
and the increase in protein synthesis, but only up to a certain
amount of ingested protein. Thus, studies indicate that there is
a relatively linier correlation between amount of dietary protein
obtained in connection with resistance exercise and increase in
protein synthesis, though it is also evident that this correlation
plateaus out at around 20 g of ingested protein (for an 85 kg
human male) and that any increase in protein intake above this
20 g limit will have no significant influence on protein synthesis
rate (Moore et al., 2009; Tang and Phillips, 2009). Furthermore,
there is evidence that protein in conjunction with resistance
training will increase the length of time in which the increase
in protein synthesis is elevated, compared to a situation in
which resistance training is carried out with no protein supplementation, or in which protein is provided but no resistance
c10.indd 126
exercise is conducted (Bohé et al., 2001; Kumar et al., 2009a,
2009b; Miller et al., 2005).
Consensus on the timing of ingestion of protein in connection with resistance training is not evident at present. Several
studies have claimed that ingestion right before and immediately after exercise is somewhat superior to the alternative in
enhancing protein synthesis. It is likely that the difference
between the two models is relatively small. The key point is
still to have the supply of protein in close connection with
the exercise training (reviewed in Kumar et al., 2009a). On the
other hand, most available evidence suggests that a delay in the
ingestion of protein will diminish the protein synthesis. A delay
of at least two hours has proved significantly less efficient than
ingestion immediately after training in long-term manifestation
of muscle fibre hypertrophy (Esmarck et al., 2001).
Very recent data elucidate the correlation between resistance
training intensity and the magnitude of increase in protein synthesis. In one resistance training study the same total amount
of work was preformed with both relatively low resistance
(20–40% of 1RM) and very high resistance (∼90% of 1RM).
Both types of training evoked an increase in protein synthesis,
but although the same total amount of work was performed, the
20–40% of 1 RM training gave a significantly smaller increase
in protein synthesis than training in the 60–90% of 1 RM area
(Kumar et al., 2009b). Interestingly, it seems as if there is a
plateau of the increased protein synthesis in the 60–90% of 1
RM area, which in practical terms mean that if one is training
with the prime aim of increasing muscle mass, from a protein
synthesis viewpoint there is no major difference between training at 60% of 1RM and at 90% of 1RM. In practical terms it is
already an established ‘truth’ among coaches and athletes that
the optimal training intensity for muscle hypertrophy is somewhere in the above-mentioned area. The novel information is
that we can now confirm this and furthermore establish that the
intensity as such probably doesn’t play a major role so long as
it is between ∼60 and 90% of 1 RM.
Another recent study on the response of muscle protein
synthesis after resistance training seems to add to our knowledge of the differences between the trained and the untrained
state. In this study a group of young male subjects conducted
resistance training exclusively for one leg, while the other leg
served as an untrained control (Tang et al., 2008). After eight
weeks the trained leg showed significant hypertrophy as well
as increased strength. Interestingly, a measurement of protein
synthesis in the two legs showed significant differences. The
untrained leg had a lower initial increase in protein synthesis
than the trained leg when submitted to resistance exercise, but
the protein synthesis of the untrained leg was still significantly
elevated 28 hours after exercise, in contrast to the trained leg,
in which the protein synthesis at this point in time was no longer
elevated from pre-exercise values. The conclusion is that the
protein synthesis in the trained muscle reacts promptly and
strongly, but fades faster than that in the muscles of the untrained
leg, given equal relative amounts of resistance training (Tang
et al., 2008). Thus, this reaction pattern is in agreement with
the general concept of reaction to ‘stress’, in the sense that a
muscle that is accustomed to stress (exercise) will react promptly
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CHAPTER 2.2
STRUCTURAL AND MOLECULAR ADAPTATIONS TO TRAINING
but also deal with the stimulus faster. Similar results have been
obtained when comparing muscle protein turnover in subjects
accustomed to resistance training versus untrained subjects
(Phillips et al., 1999). A general rule seems to be that, although
high in the early phase, the overall protein synthesis in a trained
muscle after resistance training is less than in an untrained
muscle, but protein degradation is less after resistance training
in trained muscle compared to untrained muscle.
A study design aiming to examine the differences between
resistance and endurance training in the trained and untrained
state has provided additional information on muscle protein
synthesis patterns after various types of training (Wilkinson et
al., 2008). In this study Wilkinson et al. found that protein
synthesis of both the myofibrillar and the mitochondrial protein
fractions increased after resistance training in the untrained
state, whereas in the trained state only the synthesis of the
myofibrillar proteins increased. After endurance training only
the synthesis of the mitochondrial proteins increased, in both
the trained and the untrained state. Several different interpretations of these differences in reaction pattern in protein synthesis
and degradation are possible, but one might be that the trained
muscle needs, and can tolerate, more frequent stimulus than the
untrained muscle in order to respond in a favourable manner.
Furthermore, the anabolic response of resistance training is
reduced with increased training. These results also imply that
the frequency and intensity of resistance training need to
increase progressively as the muscle becomes better trained, to
keep up the well-trained homoeostasis of the muscle. Finally,
as concluded by Wilkinson et al. (2008) and later expanded
upon by Kumar et al. (2009a), chronic resistance exercise can
modify the protein synthesis response of the protein fractions
towards an exercise phenotypic response, or as Wilkinson et al.
put it, ‘These findings provide evidence that human skeletal
muscle protein synthetic response to different modes of exercise
is specific for proteins needed for structural and metabolic adaptations to the particular exercise stimulus, and that this specificity of response is altered with training to be more specific’
(Wilkinson et al., 2008).
2.2.3
MUSCLE HYPERTROPHY
AND ATROPHY
Often the entire increase in strength in the early phase of a
resistance training programme initiated in untrained subjects is
contributed to adaptations of the neural drive (Aagaard et al.,
2002; Gabriel, Kamen and Frost, 2006). There is no doubt that
significant modifications in the nervous system in the first
weeks of heavy resistance training occur, initiating strength
gains. The question is whether these changes alone are responsible for the increased strength or whether muscle hypertrophy
kicks in almost immediately and contributes to the strength gain
after days or a few weeks of training. Most experiments can’t
show a significant increase in muscle hypertrophy earlier than
four weeks into a training programme, and often six to eight
weeks are need before the hypertrophy becomes significant
c10.indd 127
127
(Staron et al., 1994). No doubt the main contribution to strength
gain in the early phase arises from the neuromuscular adaptations, but it is somewhat strange that no muscle hypertrophy
should happen before four to eight weeks of intensive training
when it can be shown through acute studies that protein synthesis is significantly upregulated and a positive net protein balance
occurs hours after a single exercise bout (Kumar et al., 2009a).
Likewise, signalling factors that vouch for muscle hypertrophy
are increased within the same time frame (Bickel et al., 2005;
Bodine, 2006; Coffey and Hawley, 2007; Favier, Benoit and
Freyssenet, 2008).
Some newer studies may cast additional light on the problem.
In a study by Seynnes, de Boer and Narici (2007), a small group
of subjects were followed closely at the very beginning of a
strength training programme. In this study hypertrophy measured via MRI was registered after just 20 days of training, and
it could be calculated that the rate of muscle hypertrophy in the
20-day period was as much as 0.2%/day. In the same period the
overall gain in MVC was in the magnitude of ∼1%/day (Seynnes,
de Boer and Narici, 2007). Unfortunately, no muscle biopsies
were obtained and thus no measurements of hypertrophy in the
individual muscle fibres are available. Another study involving
resistance training over an eight-week period showed hypertrophy of the type II fibres, but not of the type I fibres, after four
weeks of training (Woolstenhulme et al., 2006), but overall the
studies reporting significant hypertrophy in fibre level after less
than four weeks are scarce. Even though fibre hypertrophy can’t
be documented significantly in the first weeks of training, this
doesn’t mean that it doesn’t occur. One could get the idea that
the problem lies not so much in the fact that there is no hypertrophy in the very early phase of a strength training programme,
but that we are not able to measure a potential hypertrophy in
a sensitive and sufficiently accurate manner. Calculations based
on the magnitude of fibre hypertrophy registered at week 8–12
into a resistance training programme imply that the contribution
of hypertrophy to increase in muscle strength in the initial phase
could be as much as ∼20% (Seynnes, de Boer and Narici, 2007).
Hypertrophy may not always be what is required when
strength training is conducted, but quite often it is. Strength
training in all its forms, performed with a reasonable amount
of load, will in the untrained or moderately trained muscle
inevitably lead to some muscle hypertrophy, but it is equally
clear that different types of training regimens don’t lead to the
same amount of hypertrophy. It seems as if the relative loading
of the muscle is very important to the outcome. In a review, Fry
(2004) estimates that 18–35% of the variance of the hypertrophic outcome after strength training is determined by the
relative intensity of loading during exercise, estimated from
studies using a loading between 40 and 95% of 1 RM. The
variance is greater in the type II fibres (35%) than in the type I
fibres (18%). Nevertheless, overall ∼25% of the hypertrophic
response in a mixed human skeletal muscle is determined by
the loading. This underscores the fact that loading is one of the
most (probably the most) important factors when designing
strength training programmes, both if the prime goal is increased
muscle mass and if it is increased muscle strength with as little
increase in muscle mass as possible.
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If the prime goal were hypertrophy, what would be the
optimal relative loading? Data suggest that maximal hypertrophy occurs with loads from 80 to 95% of 1 RM (Fry, 2004). As
mentioned earlier, the maximal protein synthesis seems to occur
over a broad range from 60 to 90% of 1 RM. At first glance it
could seem that there is a minor divergence between the range
of maximal hypertrophy and highest protein synthesis, especially in the ‘low’ relative loading area. Can we explain this?
Working at 60% of 1 RM would typically result in three to six
times (variable with different exercises) more repetitions for the
muscle per exercise than working at 90% of 1 RM. Thus, the
total number of contractions per training session is much higher
for the ‘low’ loads compared to the high loads. If we assume
that the two different training sessions increase protein synthesis equally (which most data from the literature seem to imply),
and the release of intrinsic growth factors within the muscle is
in the same magnitude (which may be more questionable, but
is poorly described in the literature), then the difference between
the outcomes of the two different training regimens could arise
from differences in protein degradation. Maybe the higher
number of contractions conducted in the area around 60% of 1
RM provides more wear and tear on the contractile proteins,
leading to a greater protein breakdown than the fewer contractions in the 80–95% of 1 RM area, resulting in slightly less net
protein synthesis. So far this is only speculation and to this
author ’s knowledge the two scenarios have not been tried out
in the same study (involving measurement of both protein synthesis and muscle fibre hypertrophy) in a manner that could
substantiate these speculations.
Relative loading is a very important factor in strength training. Variables such as type of exercise, order of exercises, total
volume of exercises, and rest between sets and training sessions
can all be regulated in a training regimen (Fleck and Kraemer,
2004). Likewise, variables such as speed of contraction, contraction time per rep, working to failure or not, the choice
between exercising in machines or with free weights, and
overall periodization principles will also influence the end result
(Fry, 2004). To work all these factors into a general equation
is very difficult, if not impossible, although interesting attempts
have been made to illustrate how apparently similar training
regimes can be very different when some of the abovementioned parameters are modulated (Toigo and Boutellier,
2006). Another important factor is the number of repetitions
conducted per exercise or training session; by linking this with
loading some simple rules of adaptation of the muscle can be
made. High load/low reps will provide the greatest increase in
strength the fastest, compared to medium load/medium reps and
low load/high reps. Hypertrophy might be a little higher with
high load/low reps compared to medium load/medium reps,
though not necessarily much higher, but certainly higher than
in low load/high reps (Campos et al., 2002; Fry, 2004).
As described above, strength training will in most situations
lead to muscle hypertrophy, but as is also evident, that the
amount of hypertrophy is dependent on how the training is
conducted. It has become evident that strength training does not
affect the different muscle fibre types equally; the relative
loading will determine how much the different fibre types are
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influenced. Heavy resistance training over an extended period
(e.g. three months) will initiate hypertrophy in the range of
5–15% in slow type I fibres and 15–25% in fast type II fibres
(Andersen and Aagaard, 2000). Data on the magnitude of relative hypertrophy found in the literature vary, depending on the
amount and type of strength training conducted, as well as on
the starting point of the subjects examined. Nevertheless, a
rough estimate is that the fast type II fibres will hypertrophy
twice as much as the slow type I fibres. Since fast type II fibres
cover a larger relative cross-sectional area of the muscle, the
end result is not only a stronger muscle but also a faster muscle.
In this scenario it is assumed that no major change in fibre-type
distribution occurs, a matter that we shall return to. But there
is a twist to the story: when studies using different amounts of
relative loading are compared (Fry, 2004), it becomes evident
that hypertrophy increases as the relative loading increases,
apparently following a linear regression line, though this regression line is different for the two major fibre types. The increase
in hypertrophy in the slow type I fibres observed as the loading
increases appears as a gentle line, whereas the increase in
hypertrophy seen in fast type II fibres follows a steeper line.
Thus, the difference in hypertrophic response between the two
major fibre types increases as the loading increases (Fry, 2004).
Undoubtedly the same amount of training will evoke less hypertrophy in already well (strength) trained subjects. Thus, the
background of the individual who undertakes the strength training is important.
When planning strength training for an athlete or a patient
it is important to know and take into account their training
background: a certain amount/volume of training might introduce significant muscle hypertrophy in an athlete or a patient
with no prior strength training experience, whereas an athlete
who has undertaken large amounts of resistance training might
experience regular atrophy of their muscles if they conduct the
same amount and type of resistance training prescribed for a
less experienced person, simply because the stimulus to their
muscles and nervous system will be less intense than the
muscle–CNS signalling that they normally receive. One of the
key points of a hypertrophied muscle is that it is not in equilibrium and will strive towards a less hypertrophied status if the
stimulus is lowered or removed. Thus, the ‘problem’ that many
athletes face is centred around questions like: How do I counteract atrophy form a very hypertrophic state during the competition period? How fast does the hypertrophied muscle
decrease (and it does) if I remove the resistance training? How
much training is enough the keep up the gained strength and
hypertrophy, or at least to minimize the loss? These are questions that should be addressed more closely in the coming years.
2.2.3.1 Changes in fibre type
composition with strength training
We know that a muscle’s ability to conduct a fast and forceful
contraction contributes positively to performance in certain athletic events. Within muscle physiology it has been know for
many years that the maximum speed at which a muscle can
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contract is to a large extent given by the its composition of fast
and slow muscle fibres (Bottinelli and Reggiani, 2000; Harridge,
1996). Likewise, the maximum force and power produced by
the single muscle fibre is strongly positively related to its
content of fast myosin (Bottinelli et al., 1999), which can also
be observed during in vivo muscle contraction in the intact
human (Aagaard and Andersen, 1998).
Human skeletal muscle fibres contain different proteins
facilitating contraction. Some proteins are structural, having the
task of maintaining the physical structure of the fibre as force
is produced, whereas others are involved in the actual contractile process (Schiaffino and Reggiani, 1996). The two main
proteins involved in muscle contraction are myosin (the thick
filament) and actin (the thin filament). In the human skeletal
muscle actin only exists in a singular form. Myosin (or more
precise the heavy chain of the myosin molecule, MHC), on the
other hand, exists in three different forms (known as isoforms;
essentially different versions of the same protein taking care of
the same task) (Schiaffino and Reggiani, 1994). Each of these
MHC isoforms, when present in the fibre, provides it with
specific functional characteristics, the primary one being contraction velocity. A number of other proteins contribute or
modulate the outcome but the absolute most important determinant of the fibre’s contraction velocity is the MHC isoform
within it. The three MHC isoforms present in physiologically
relevant amounts in human skeletal limp muscles are MHC I,
MHC IIA, and MHC IIX (the latter is often referred to in
older literature as ‘IIB’; Smerdu et al., 1994) (Schiaffino and
Reggiani, 1996). Thus, muscle fibres can be separated into different fibre types with specific contraction characteristics via
identification of the MHC isoform(s) present in the individual
fibres. The three different MHC isoforms should in principle
result in three different muscle fibre types, but in the human
skeletal muscle two MHC isoforms are often present alongside
each other in the same fibre. Under normal circumstances only
MHC I/MHC IIA and MHC IIA/MHC IIX are expressed
together in the same muscle fibre. This results in five different
fibre types: fibres containing only MHC I, only MHC IIA, and
only MHC IIX, which constitute the ‘pure’ fibre types, and
‘hybrid fibres’ co-expressing MHC I and MHC IIA as well as
MHC IIA and MHC IIX. Additionally the hybrid fibres can
contain various relative amounts of the two isoforms, and thus
a continuum of fibre types from the pure MHC I to the pure
MHC IIX fibre can be found in the human skeletal muscle
(Andersen, Klitgaard and Saltin, 1994).
Maximum contraction velocity of single human skeletal
muscle fibres can be determined experimentally, and shows that
fibres containing MHC I are the slowest and fibres containing
MHC IIX are the fastest. Thus, contraction velocity for the different fibre types is: MHC I < MHC I/IIA hybrids < MHC
IIA < MHC IIA/IIX hybrids < MHC IIX (Bottinelli, 2001;
Harridge et al., 1996). The difference in maximum shortening
velocity (when determined in single fibres) between fibres containing only one of the three MHC isoforms is in the order of
magnitude of 1 : 3 : 8 (MHC I : MHC IIA : MHC IIX), where
co-expression hybrid fibres are placed in between (Fitts and
Widrick, 1996; Harridge, 2007). These data are the result of
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129
experiments conducted on isolated single fibres at relatively low
temperature (15–18 °C). Recent data conducted at more physiological relevant temperature (35 °C) seem to indicate that the
true difference is less, and in the magnitude of 1 : 2 between
MHC I and MHC II fibres (Lionikas, Li and Larsson, 2006).
A number of studies have shown a strong correlation
between fibre type composition of an intact muscle and the
velocity properties of the muscle, both in different muscles with
different fibre type compositions in the same individual
(Harridge, 1996; Harridge et al., 1996) and in the same muscle
between different individuals with different fibre type compositions (Aagaard and Andersen, 1998; Tihanyi, Apor and Fekete,
1982; Yates and Kamon, 1983). The relationship between fibre
type composition and muscle contractile velocity does not
emerge at slow contraction velocities, because slow fibres in
this situation have ample time to build force up to more or less
the same level as the fast fibres (Aagaard and Andersen, 1998).
Consequently, the close relationship between maximal concentric muscle strength and the percentage of MHC II in intact
human skeletal muscle first becomes apparent at high contraction velocities (Aagaard and Andersen, 1998). In practical terms
this mean that a person with a relatively large proportion of fast
fibres will be able to achieve higher muscle force and power
output during fast movements, including the early acceleration
phase, than a person with a low relative proportion of fast fibres.
Likewise, muscles characterized by a high relative proportion
of MHC II content are substantially more ‘explosive’ (i.e. demonstrate a greater rate of force development, RFD) than muscles
with low relative MHC II content, demonstrating an enhanced
capacity for rapid force production (Harridge et al., 1996).
With the above in mind we know that a person with a high
relative amount of MHC II, all other things being equal, will
be more suited for sports in which fast, explosive-type movements performed over shorter periods of time are crucial. It
becomes interesting to know whether it is possible through
training to change the MHC isoform composition in human
skeletal muscle.
From a huge collection of animal studies it is known that
manipulation of the MHC isoform content of muscle fibres, as
well as of the intact muscles, is possible (Pette and Staron,
2000). In humans, a number of critical conditions can introduce
large changes in MHC compositions in skeletal muscle. A
spinal cord injury leading to paralysis will after a while lead to
an almost complete abolishment of the slow MHC isoform in
the affected muscles, leaving the muscle to exclusively express
the two fast MHC isoforms (Andersen et al., 1996), which tells
us that significant switches between expression of fast and slow
MHC isoforms are possible in most skeletal muscles.
Nevertheless, the above-described scenario of a complete
change in expression from slow to fast MHC isoforms after a
spinal cord injury, along with the often drastic manipulations
used in animal studies, does not explain what happens within
the frame of ‘physical training’. What is the range of changes
in MHC isoform composition in the muscles when we do
strength training? Numerous studies have shown that heavyresistance exercise training will decrease the expression of
MHC IIX in human skeletal muscle and simultaneously increase
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the expression of MHC IIA, whereas the expression of MHC I
is less affected (Adams et al., 1993; Andersen and Aagaard,
2000; Hather et al., 1991). This is a solid observation and a
general consensus on this point has emerged (Fry, 2004; Folland
and Williams, 2007). Likewise, cessation of resistance training
will induce, or re-induce, MHC IIX at the expense of MHC IIA
(Andersen and Aagaard, 2000; Andersen et al., 2005). Whether
or not the number of fibres expressing MHC I is increased or
decreased after strength training is debateable, but most likely
there is no or only very subtle change in the number of fibres
expressing MHC I (Andersen and Aagaard, 2000; Fry, 2004).
Thus, the general rule of MHC isoform plasticity in human
skeletal muscle appears to be that introduction of, or increase
in, the amount of resistance training leads to a decrease in MHC
IIX and an increase in MHC IIA, while a withdrawal or decrease
in resistance training leads to an increase in MHC IIX and a
decrease in MHC IIA. MHC I seems to be relatively unaffected
by resistance training (Andersen and Aagaard, 2000; Fry,
2004).
The disappearance of MHC IIX with strength training might
seem unfavourable since this MHC isoform has the fastest contraction velocity and highest power production. Removal of
MHC IIX from the muscle should lead to a slowing and reduced
power output of the muscle. Theoretically this is the case when
looking at the isolated individual fibre, but in terms of the
capacity of the intact muscle this apparent slowing is, in most
athletic settings, more than outweighed by the increase in contractile strength, power, and RFD of the trained muscle
(Aagaard, 2004). In consequence, maximal unloaded limb
movement speed is observed to increase (Aagaard et al., 2003;
Schmidtbleicher and Haralambie, 1981) or remain unaltered
(Andersen et al., 2005) following 3–4 months of heavyresistance strength training. The increase in muscle force,
power, and RFD following heavy-resistance strength training is
to a large extent caused by the fast fibres demonstrating a
twofold greater hypertrophy than the slow fibres in response to
heavy-resistance training (Aagaard et al., 2001; Andersen and
Aagaard, 2000; Kosek et al., 2006). Moreover, a differentiated
hypertrophy of the fast and slow fibres with heavy resistance
training, in favour of the fast fibres, will eventually give rise to
not only a bigger muscle but also a muscle in which a relatively
larger proportion of the cross-sectional area is occupied by fast
fibres and there is thus also a higher relative amount of MHC
II (Aagaard, 2004; Andersen and Aagaard, 2000).
Data from our lab indicate that heavy-resistance training
followed by de-training can evoke a boost in proportions of the
MHC IIX isoform. In a strength training study examining a
group of young healthy males, we saw that the percentage of
MHC IIX in the vastus lateralis muscle of the subjects decreased
from 9% to only 2% during the three-month training period.
Interestingly, the percentage of MHC IIX subsequently
increased to 17% after an additional period of three months of
de-training (Andersen and Aagaard, 2000). Thus, the relative
level of MHC IIX after three months of de-training was significantly higher than both the level after training and the level
before the training period (Andersen and Aagaard, 2000). In a
similar study, we found that the MHC IIX boost after de-
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training was accompanied by a parallel increase in RFD in the
trained muscles (Andersen et al., 2005). However, de-training
also resulted in a loss of muscle mass to levels comparable with
those observed prior to the training period. This apparent boosting of the MHC IIX isoform with de-training (tapering) is
potentially interesting if the goal of a long-term training programme is to increase the relative amount of MHC IIX in the
muscle of a specific athlete, typically an athlete competing in
an athletic event in which no endurance work is necessary, and
contractile speed, power, and/or explosiveness (RFD) is dominantly favoured. At this point in time we do not know how the
muscle will react beyond the experimental period of three
months, but it can be expected that the level of MHC IIX
will eventually return to the original pre-training value (Staron
et al., 1991).
Is a high relative amount of MHC IIX in the major skeletal
muscles desirable in situations other than an athlete’s participation in relatively specialized compositions? It has been
established that muscle fibres containing predominantly the
MHC IIX isoform rely on a metabolism that enables them to
produce very high amounts of energy in a short time (i.e.
exerting very high power), but only over a very limited period
(seconds) (Harridge, 1996; Harridge et al., 1996). In consequence, the MHC IIX-containing fibres need to rest to avoid
exhaustion. They will not get sufficient rest in the major ball
sports (with the possible exception of e.g. American football),
or other sports in which continuous work over longer periods
are in demand. Therefore, fibres containing MHC IIA may be
preferable for athletes who compete in events in which a relatively fast but also somewhat enduring muscle is desirable;
that is, most ball games, 400–1500 m running, rowing, kayaking, cycling events like sprint and team pursuit, and so on.
Training to meet these conditions is much ‘easier ’ to plan
than training to provoke fibres to express exclusively MHC
IIX. However, if the aim is to produce a very fast 100 m or
200 m sprinter (i.e. targeting the latter training regime) then
training involving hours of continuous work at a moderate
aerobic level should be avoided, as this type of exercise can
lead to an increased number of fibres expressing MHC I
(Schaub et al., 1989) and/or fibres co-expressing MHC I and
MHC IIA. Furthermore, aerobic exercise of the above nature
may partially blunt the hypertrophic muscle response from
concurrent resistance training (Baar, 2006; Coffey et al., 2009;
Glowacki et al., 2004; Nader, 2006). Planning of the training
schedule will also have to include some type of tapering leading
up to competition.
In those cases in which some type of short-term muscle
endurance is also needed, training exercises should comprise
high-intensity intermittent work along with substantial amounts
of resistance exercise; the former gives rise to improved shortterm endurance of the MHC IIA fibres, while the latter produces
a preferential hypertrophy in the MHC II muscle fibres in
general. Ultimately, the result is a muscle which is optimized
towards the highest possible relative amount of MHC IIA at the
expense of both MHC I and MHC IIX. Of course, this scenario
favours athletes who have a relatively high amount of type II
fibres to begin with. Whether or not these type II fibres contain
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STRUCTURAL AND MOLECULAR ADAPTATIONS TO TRAINING
MHC IIA or MHC IIX at the point of origin is of less importance, since the inherent transformation MHC IIX → MHC IIA
will be introduced through resistance training.
2.2.4 WHAT IS THE SIGNIFICANCE
OF SATELLITE CELLS IN HUMAN
SKELETAL MUSCLE?
Unlike many other cell types in the human body, muscle fibres
are multinucleated. The very elongated nature of the muscle
fibres supports an organization in which each of the hundreds
or thousands of nuclei along the length of the individual fibres
governs a finite area or volume (Kadi et al., 2004, 2005; Petrella
et al., 2008). This volume is termed the myonuclear domain.
Thus, each nucleus regulates gene transcription and ultimately
protein synthesis of its specific domain. If a fibre grows, and no
new myonuclei are added, each existing myonucleus has to
support a myonuclear domain that has increased in size. All
other things being equal, this could potentially bring down
efficiency.
Myonuclei in the adult skeletal muscle cannot divide. Thus,
if there is need for supplementation of myonuclei due to damage
repair or in situations in which substantial hypertrophy is
ongoing, the individual muscle fibre needs a source of new
myonuclei. This is achieved by the satellite cells: quiescent
undifferentiated progenitor cells located outside the sarcolemma but under the basal membrane of the individual skeletal
muscle fibres (Hawke, 2005; Kadi et al., 2005). Unlike myonuclei, the satellite cells have the potential to go into mitosis and
divide. If activated, the satellite cells will proliferate and replace
damaged myonuclei or supplement the existing pool of myonuclei. There is substantial evidence to suggest that satellite cells
have a capacity for asymmetric cell division to allow for selfrenewal in order to maintain the precursor pool (Conboy and
Rando, 2002). In practical terms this means that when an activated satellite cell divides, one of the two new cells will return
to a quiescent state, ready for a new division, while the other
one will proceed to become a valid myonucleus, taking part in
the machinery of the muscle fibre to which it belongs.
Furthermore, in some situations satellite cells have the potential
to deliver nuclei for the formation of new muscle fibres.
This process has become evident in animal studies, in which
damage of adult muscle fibres evokes a neoformation of muscle
fibres (Hawke, 2005). Whether such a neoformation occurs
after extensive resistance training is still unclear and a matter
of speculation. Thus, whether or not a potential neoformation
has any physiological significance in the general muscle hypertrophy of resistance-trained human skeletal muscle is debateable, but most likely satellite cells only facilitate formation of
new segments in already existing damaged fibres, as well as
delivering additional myonuclei to already existing muscle
fibres, without adding truly new fibres.
Today it is possible, in human skeletal muscle biopsies, to
stain and count the number of myonuclei as well as the number
of quiescent and activated satellite cells, and with a relatively
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131
high certainty to separate the three (Mackey et al., 2009). Using
different markers unique to either myonuclei or quiescent and
activated satellite cells in combination with the physical location of the nucleus, it has become evident that resistance training is a potent stimulus for the activation of skeletal muscle
satellite cells (Kadi et al., 2004, 2005; Mackey et al., 2009;
Petrella et al., 2008).
We have conducted a study in which we biopsied the vastus
lateralis muscle of a group of young men during 90 days of
heavy-resistance exercise training followed by 90 days of detraining (Kadi et al., 2005). We observed muscle fibre hypertrophy of ∼6% after 30 days and ∼17% after 90 days of training.
Likewise, an increased number of satellite cells could be
observed in the training period, followed by a return to pretraining values in the de-training period. The interesting part
is that even though it was possible to show an activation of
the satellite cells, it was not possible to measure an increase
in the number of myonuclei during either the training or the
de-training period. Thus, it might be that the satellite cells
were activated, proliferated, but not differentiated. At least the
new satellite cells did not end up as a measurable increase in
myonuclei (Kadi et al., 2005). Thus, it seems as if each myonucleus was able to support a larger cytoplasmic area; consequently the size of the myonuclear domains was increased
(Kadi et al., 2004). These data, along with other similar findings (Petrella et al., 2006) seem to imply that a certain amount
of hypertrophy of the muscle fibres can be managed by the
existing myonuclei simply by expanding their myonuclear
domains. The question is, what happens if the hypertrophic
stimulus continues and hypertrophy of the existing fibres
expands beyond the ∼20% observed in our study?
Data from several research groups suggest that a limit of
hypertrophy in the magnitude of ∼25% seems to constitute
some kind of ceiling: a ceiling that has to be broken before a
regular and significant increase in the number of myonuclei sets
in (Kadi et al., 2004, 2005). Petrella et al. (2006) have suggested this ceiling could be around 2000 μm2 per nucleus.
A very recent study has shed new light on this myonuclear
domain ceiling. In this study a relatively large group of subjects
performed 16 weeks of hypertrophy-inducing resistance training (Petrella et al., 2008). Afterwards the subjects could be
subdivided into three groups, having muscle fibre hypertrophy
of ∼50%, ∼25% and ∼0%. Of course, the group with no or very
little hypertrophy did not reach the myonuclear domain ceiling.
The ∼25% group expanded the myonuclear domain up to
2000 μm2 per nucleus, while the ∼50% group showed a myonuclear ceiling domain of 2250 μm2 per nucleus. These data indicate that any potential myonuclear ceiling domain is likely to
vary from person to person (Petrella et al., 2008). Moreover,
the study showed that the availability of satellite cells in the
untrained muscle is important to the hypertrophic potential,
since the ∼50% group had significantly more satellite cells in
their vastus lateralis muscle prior to training; in addition they
were able to expand the pool of satellite cells by a greater
amount than the two other groups.
Together, these studies may provide some explanation as
to why muscles in different individuals hypertrophy at very
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different rates even when subjected to exactly the same training
stimulus.
On the speculative level, the whole concept of a myonuclear
domain ceiling can lead to a muscle fibre hypertrophic scenario
that follows a gearing pathway. First gear is the initial phase,
in which the muscle fibre increases the size without any major
increase in new myonuclei; this phase involves relatively fast
hypertrophy, indicating that an increase in the net protein synthesis is managed by the already existing machinery. Second
gear sets in when the myonuclear ceiling domain is reached; in
this gear the continuing hypertrophy develops more slowly
since new myonuclei have to be incorporated in order to further
expand growth. In the late stage of the hypertrophic process the
muscle fibres drive in both gears simultaneously. It should be
noted that the proliferation for the later differentiation of the
satellite cells appears to start early in the initiation phase of the
resistance training programme, preparing the muscle fibre for
the situation that might arise in the future (Petrella et al., 2008).
On an even more speculative note, it could be imagined that the
period in which the gearshift happens could involve a plateau
in the hypertrophy.
Of interest in the study by Petrella and co-workers (Petrella
et al., 2008) is the observation that the proliferation of satellite
cells far surpassed the myonuclear addition in the ∼50% group.
It is suggested that this ‘overproduction’ of satellite cells could
lead to a stockpile of precursor satellite cells. Such a stockpile,
if kept available and not discarded, could act as a potential
booster in a situation where resistance training is resumed after
a period with no or very limited resistance training, explaining
at least in part the phenomenon known as ‘muscle memory’.
Muscle memory is the observation among bodybuilders and
strength athletes that if one has already been through a period
of intense hypertrophic-inducing training, it is ‘easier ’ to get
this hypertrophic effect again, after a period of loss of muscle
mass, than it is when starting from scratch. On the other hand,
our own studies seem to indicate that the number of satellite
cells is not increased above baseline in the de-training phase
(Kadi et al., 2005), which speaks against the idea of the stockpile of satellite cells. Thus it is more likely, but difficult to
verify, that the existing satellite cells store some knowledge of
earlier damage or stress (for lack of a better way of putting it)
that makes them react more rapidly the second time they are
subjected to the resistance training stimulus.
2.2.5
CONCURRENT STRENGTH AND
ENDURANCE TRAINING:
CONSEQUENCES FOR
MUSCLE ADAPTATIONS
Very few sports are solely strength-related, for example almost
all ball games require skills related to muscle strength but also
demand high anaerobic and aerobic capacity. Thus, physical
training for these sports involves a combination of strength and
endurance qualities. Of course, focus can be placed on one or
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the other, but the total training effort will always reflect the need
for both. Although there is overlap in the molecular response
of the skeletal muscle to endurance and resistance training, it
has become evident that skeletal muscle is capable of distinguishing between the intensity, duration, and nature of contractions (Kumar et al., 2009a).
A substantial number of studies have tried to examine how
concurrent strength and endurance training might influence the
adaptation of either quality compared to conducting the two
types of training separately. Given the topic of this chapter, it
is important to try to elucidate how concurrent endurance training will affect the strength and hypertrophy response that is
initiated by strength training alone. Although not new, the question is still difficult to answer. Nevertheless the arrival of
molecular biology has given rise to some possible explanations
for a few of the adaptive responses that can be seen in long-term
training studies (Bell et al., 2000; Glowacki et al., 2004;
Häkkinen et al., 2003; Izquierdo et al., 2005; Kraemer et al.,
1995). Around 1980 Robert C. Hickson published a number
articles opening up the area scientifically. He suggested that
conducting concurrent strength and endurance training didn’t
affect the adaptation of cardiovascular qualities (VO2max etc.)
(Hickson, 1980), and later experiments have shown that endurance performance is likely to benefit from concurrent strength
training if it is conducted in the right manner (Hoff, Helgerud
and Wisløff, 1999; Østerås, Helgerud and Hoff, 2002;
Rønnestad, Hansen and Raastad, 2009; Støren et al., 2008).
Hickson also showed that concurrent strength and endurance
training was likely to at least dampen some of adaptations in
muscle strength and hypertrophy when compared to strength
training alone (Hickson, 1980). Long-term studies conducted
since have to a certain extent reached conclusions along the
same lines (Häkkinen et al., 2003).
What has been more difficult to explain is how signalling
pathways in the muscle following endurance training might
inhibit the signalling pathway initiated by resistance training.
Probably the most robust explanation revolves around a
complex of regulation pathways with offspring in the activation
of the AMPK pathway through endurance training; this seems
to block the Akt/mTOR pathway, which is partly responsible
for the increase in protein synthesis and eventual hypertrophy
after resistance training (Bodine, 2006). This idea was first
developed in animal models (Baar and Esser, 1999; Bodine et
al., 2001; Haddad and Adams, 2002; Pallafacchina et al., 2002)
and later in human training models (Baar, 2006; Bodine, 2006;
Coffey and Hawley, 2007; Nader, 2006; Rivas, Lessard and
Coffey, 2009). We now know that concurrent endurance training to some extent compromises the benefits of resistance training. Nevertheless, it is obvious that many athletes have to
conduct endurance training along with strength training in order
to fulfil the demands of the sport in which they are competing.
The next question is, how do we plan concurrent training so
that we get the most out of the invested effort? For example, if
both qualities are trained on the same days, what would be the
preferred order if muscle hypertrophy were to be given high
priority? A very recent study has looked at concurrent endurance and strength training and how the order in which the
10/18/2010 5:11:31 PM
CHAPTER 2.2
STRUCTURAL AND MOLECULAR ADAPTATIONS TO TRAINING
training is conducted affects stimuli at the mRNA level. In this
study a group of reasonably well-trained male subjects was, on
different days, subjected to either endurance training followed
by resistance training or vice versa, in a cross-over design.
Muscle biopsies were obtained prior to exercise, after the first
exercise bout, after the second excise bout, and again three
hours post-exercise (Coffey et al., 2009). The experiment
shows that the phosphorylation of mTOR is downregulated in
the post-training phase if endurance training is undertaken after
strength training, potentially downregulating protein synthesis.
If endurance training is undertaken first, this is not the case.
Furthermore, phosphorylation of Akt1 is upregulated after
resistance training (positive for protein synthesis), but what is
interesting is that a post-endurance training bout does not
prevent a later increase in Akt1 phosphorylation initiated by the
subsequent resistance training bout. Furthermore, the experiment shows that mRNA for the two ubiqutin ligases, Atrogin
and MuRF, which target protein for later degradation and thus
create an environment of increased protein degradation,
increases when endurance exercise is undertaken after resistance exercise; the reverse is true when the exercise bouts are
carried out the other way around. Together, these data seem to
indicate that resistance training should be conducted after
c10.indd 133
133
endurance training if the purpose is to provide better circumstances for an overall positive ratio in the protein synthesis/
degradation balance.
Although there is still a great deal of work to be conducted
in the area of concurrent endurance and resistance training, a
picture is starting to form. (1) If endurance training is undertaken prior to resistance training then there is a possibility that
the hypertrophic response seen with resistance training will
only be somewhat diminished, but the overall negative effect
might be relatively small and thus only relevant when the the
focus is on muscle hypertrophy. (2) If resistance training is
conducted prior to endurance training then there is an effect on
the hypertrophic stimulus provided through the resistance training; furthermore, studies seems to indicate that the break on the
hypertrophic response, most likely through accelerated protein
degradation, is more pronounced than when endurance training
is conducted prior to resistance training.
As a preliminary conclusion our advice to athletes is: end
your concurrent training session with the type of training that
has the highest priority. For example, athletes who train with
the purpose of optimizing muscle strength and muscle hypertrophy, but still need to conduct concurrent endurance training,
should carry out their resistance training last.
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10/18/2010 5:11:31 PM
2.3 Adaptive Processes in Human
Bone and Tendon
Constantinos N. Maganaris, Jörn Rittweger and Marco V. Narici, Manchester Metropolitan University, Institute for
Biomedical Research into Human Movement and Health (IRM), Manchester, UK
2.3.1
INTRODUCTION
Bones and tendons have certain structural and functional similarities. Both materials are composites and are subjected to
forces generated during joint movement and locomotion, and
both exhibit mechanical behaviour adaptable to the conditions
of functional loading they experience.
The plasticity of bones is a characteristic relevant to the
management of fractures, a major concern in old age worldwide
(Baron et al., 1996; Gullberg, Johnell and Kanis, 1997). The
fracture risk in older people is, at least partly, due to the
reduction in bone material (Kanis et al., 2001), and also to
deterioration of the bone material’s intrinsic properties (Diab
et al., 2006; Nalla et al., 2004; Shiraki et al., 2008). The term
‘osteoporosis’ summarizes these bone-related alterations that
predispose to fractures. As discussed in detail in Chapter 1.3,
bones can adapt to mechanical stimuli by adding material
where it is needed and removing it where it is dispensable.1
Hence, one might expect that ‘increasing’ the mechanical
stimulation of bone should lead to ‘bigger ’ and stronger bones.
Accordingly, exercise should constitute a straightforward
means to prevent osteoporosis and fractures (Kohrt et al., 2004;
Rittweger, 2006).
The first part of this chapter will discuss the extent to which
this is achievable and address the issue of how exactly bones
behave in response to mechanical loading in the form of exercise and physical activity, or the lack of it. The second part of
the chapter is dedicated to tendons, which also adapt to the
presence or absence of mechanical loading and change their
properties accordingly. This part will discuss in detail the functional role of tendons and review recent knowledge on the
application of in vivo techniques for quantifying human tendon
mechanical properties and their adaptations to mechanical
1
Bone material properties, by contrast, seem to be fairly constant within
species; see Currey (2002), Ruffoni et al. (2007).
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
c11.indd 137
loading in the form of strength training and chronic physical
activity, or chronic unloading caused by pathology and experimental manipulation in healthy humans.
2.3.2 BONE
2.3.2.1 Origin of
musculoskeletal forces
Mechanical engineers design structures so that they can safely
tolerate the peak loads applied to them. Biomechanical analyses
suggest that the peak forces in our musculoskeletal system
are generated by muscle contractions, rather than by gravitational loading. This is illustrated for the human ankle joint in
Figure 2.3.1.
In hopping, walking, and running, loads are typically
applied through the ball of the foot. As illustrated in Figure
2.3.1, the tensile force generated by the calf muscles and transmitted through the Achilles tendon is three times larger than
the ground reaction force.2 As a consequence, the gravitational
forces of the body weight are small in comparison to the forces
generated by muscle contractions. This is due to the fact that
our muscles work against short levers, ranging between 1 : 2
to 1 : 10 (Martin, Burr and Sharkey, 1998; Özkaya and Nordin,
1998). The situation is even more aggravated in the upper
extremity, where body weight does not usually contribute at
all to the loading of bones. In this context, the concept of
‘weight bearing’ seems dispensable, or even misleading.
Rather, we have to acknowledge that it is the muscular forces
that the skeleton has to adapt to. In the lower extremity, those
2
We are considering only the net moments and forces here. In reality, one has
to assume that the antagonistic muscle groups will be co-contracting at the
same time (see Baratta et al., 1988), and that the calf muscle and tendon forces
are consequently larger than those net forces.
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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3.5
18Y
Bone Mineral Content [kg]
3
2.5
18Y
15Y
2
12Y
1.5
1
0.5
Males
Females
2Y
0
0
10
20
30
40
Lean Body Mass [kg]
50
60
Figure 2.3.2 Muscle–bone relationship, as assessed by whole-body
dual x-ray absorptiometry. Bone mineral content (BMC) and lean
body mass (most of which is muscle mass) are directly proportional
to each other in boys between 2 and 15 years of age, and in girls
between 2 and 12 years of age. After the onset of puberty, this
relationship is lost in girls, who accrue more BMC than is explicable
by lean body mass. Data from Zanchetta, Plotkin and AlvarezFilgueira (1995) and adopted according to Schiessl, Frost and Jee
(1998)
Figure 2.3.1 Biomechanical analysis of the loading patterns around
the ankle joint. The force introduced via the ball of the foot operates
a lever that is approximately three times longer than the Achilles
tendon. Therefore, the Achilles tendon force will be three times larger
than the ground reaction force (indicated by the black arrows). If we
neglect the mass of the foot and the lower shank, another force
component will be transmitted through the tibia to support the body
mass (indicated by the fourth white arrow). Peak ground reaction
forces during one-legged hopping range around 2.5 kN in young men
with 70 kg body mass (Runge et al., 2004). Accordingly, the calf
muscles generate a force of 7.5 kN, and the tibia is loaded with 10 kN
(equivalent to the weight of one tonne). Weight, on the other hand, is
defined as mass × gravitational acceleration. Hence, the force
contribution to the loading of the tibia, as by the body weight, is
70 kg × 9.81 m/s/s, or 0.7 kN, or only 7% of the total loading
muscle forces are obviously generated with body mass as an
inertial resistor.
Evidence suggests that the tibia strength is indeed adapted
to calf muscle cross-section as a surrogate measure of muscle
strength (Rittweger et al., 2000). More generally, there seems
to be a stoichiometric relationship between musculature and
skeleton in the human body, as demonstrated in Figure 2.3.2. It
can also be seen from this figure that during puberty girls start
c11.indd 138
to accrue more bone mass than explicable by muscle mass. It
seems reasonable to assume that this surplus constitutes a
calcium reservoir to be utilized during lactation (Kalkwarf and
Specker, 1995; Kalkwarf et al., 1996; Schiessl, Frost and Jee,
1998).
The question arises how many, and what kind of, deformation cycles are required to optimally build stronger bones. In
growing rats (Umemura et al., 1997), but also in the turkey ulna
(Rubin and Lanyon, 1987), four to five cycles per day seem to
elicit a maximal or near-maximal response. On the other hand,
it has been argued that many cycles of comparatively small
deformation magnitude can have the same effect upon bone as
a large number of relatively small deformations (Rubin et al.,
2001). Moreover, strain rate is known to affect bone adaptive
processes independent of strain magnitude (Mosley and Lanyon,
1998). It is of interest in this context that muscles themselves
generate higher-frequency components (Huang, Rubin and
McLeod, 1999), and that the rate of force development by a
muscle varies across individuals and contraction types, as for
example in different kinds of sports.
2.3.2.2 Effects of immobilization
on bone
Immobilization leads to rapid and profound bone losses. This
is best demonstrated in individuals with spinal-cord injury
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ADAPTIVE PROCESSES IN HUMAN BONE AND TENDON
3
4
Close to the joints.
The shafts of long bones.
c11.indd 139
(a)
139
Time course of recovery
1
0
Change from Baseline [%]
(SCI), where muscles are paralysed due to nervous traffic disruption. Biochemical markers of bone resorption are strongly
increased immediately after the injury (Maimoun et al., 2005),
returning to baseline values within a few years (Reiter et al.,
2007; Zehnder et al., 2004). Importantly, the bone losses occur
only in the paralysed limbs (Biering-Sorensen, Bohr and
Schaadt, 1990; Frey-Rindova et al., 2000; Tsuzuku, Ikegami
and Yabe, 1999), and a new steady state is reached after approximately five years (Eser et al., 2004). The losses are more
pronounced in the epiphyses3 than in the diaphyses4 (Eser et al.,
2004). It should be realized that some muscle contractions still
take place in the paralysed limbs, and it has been proposed that
the residual state reflects bone adaptation to the musculature’s
force-generating potential (Rittweger et al., 2006b). In that
sense, one can interpret the bone losses after SCI as an adaptive
process.
Similarly, bone losses are observed in many other clinical
disorders, such as stroke (Jorgensen et al., 2000) and anterior
cruciate ligament (Leppala et al., 1999), as well as other
soft-tissue knee injuries (Sievanen, Heinonen and Kannus,
1996). Bone loss is also a major concern for long-term space
missions. It probably owes to the inability to elicit forceful
muscle contractions under microgravity conditions that bone
mass is readily lost during space flight (Mack et al., 1967;
Oganov et al., 1992; Rambaut et al., 1975); experimental bed
rest is a ground-based model to simulate this (LeBlanc et al.,
1990; Rittweger et al., 2005a; Vico et al., 1987). The past
decade has seen vigorous efforts to develop countermeasures
against such immobilization-induced bone losses (Pavy-Le
Traon et al., 2007). Research has yielded unfavourable results
for endurance exercise (Grigoriev et al., 1992), and for resistive exercise when it is only performed for two to three days
per week (Rittweger et al., 2005a; Watanabe et al., 2004).
However, when performed on a daily basis, resistive exercise
with (Rittweger et al., 2010) or without (Shackelford et al.,
2004) whole-body vibration (WBV) has proved to be highly
effective.
Bone losses incurred during bed rest are recovered within
one or two years (Rittweger and Felsenberg, 2009). This
recovery is remarkable in three ways. First, the accrual is
initially extremely rapid (see Figure 2.3.3a), comparable to
the pubertal growth spurt in quantitative terms. Second, the
recovery is stimulated by merely habitual activity and does
not require specific measures. The ease with which bone is
accrued during rehabilitation is therefore in stark contrast to
the hardships of preventing bed rest-induced bone losses by
regular exercise (Rittweger et al., 2006a), and also to the
difficulty of increasing bone mass by regular training (see
Section 2.3.2.3). Third, the bone mineral gained during the
recovery period matches exactly the losses incurred during
bed rest (see Figure 2.3.3b). This is the more surprising as
bed rest-induced bone losses show great inter-individual variability. It therefore seems that bone adaptation is both highly
efficient and tightly controlled.
-1
-2
-3
-4
-5
-6
-7
0
3
6
9
12
Follow-up [Months]
Individual Values
(b)
20
Identity
Linear
(BMC_pCC_HDT89)
15
Accrual during follow-up
CHAPTER 2.3
10
5
0
5
0
-5
-10
-15
-20
-5
Bed rest-incurred loss
Figure 2.3.3 Recovery of losses in bone mineral content that
occurred in the distal tibia epiphysis in response to 90 days of strict
bed rest. Diagrams have been adopted from Rittweger and Felsenberg
(2009). (a) Values are given as percentage changes from baseline for
the control group (Ctrl), which did bed rest only, without any
exercise, and for the group that did resistive exercise on a gravityindependent dynamometer two to three times per week (Ex). A
curvilinear time course of recovery was perceivable in all individuals.
It has been fitted here by an exponential function, compatible with a
first-order regulatory system. (b) Comparison of intra-individual
losses at the end of bed rest and the accrual of bone mass during 12
months’ follow-up after the bed rest. As can be seen, the two were
closely correlated (R2 = 0.87), indicating that re-accrual individually
matched previous losses. Upper curved line = Ex; lower curved
line = Ctrl
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2.3.2.3
PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
Effects of exercise on bone
It is widely held that exercise is beneficial for bone health
(Kohrt et al., 2004). This view is based on a great number of
interventional studies that have demonstrated increases in
bone strength through physical exercise (Bassey et al., 1998;
Friedlander et al., 1995; Heinonen et al., 1996; Lohman et al.,
1995; Maddalozzo and Snow, 2000; Snow-Harter et al., 1992;
Vincent and Braith, 2002). Importantly, the exercise effects are
site-specific (Adami et al., 1999; Bass et al., 2002; Heinonen
et al., 1996; Kannus et al., 1994; Kontulainen et al., 1999;
Johannsen et al., 2003; Winters-Stone and Snow, 2006); that is,
they occur in the loaded bones only.
Bone adaptation consists in structural modification, rather
than alteration of bone material properties (Haapasalo et al.,
2000). As such, there is an increase in area and cross-sectional
moment of inertia (see Chapter 1.3) of cortical bone, and also
an enhancement of the density of the trabecular (Haapasalo
et al., 2000; Nikander et al., 2005, 2006; Wilks et al., 2009a).
Quantitatively, exercise effects seem to be larger in the diaphyses than in the epiphyses. Epiphyses are rich in trabecular bone,
which might indicate that trabecular bone is in stronger relation
to endocrine and metabolic processes than cortical bone (Hagino
et al., 1993; Rittweger et al., 2009). However, it must be considered that the mechanical competence of trabecular bone
increases by the power of 2–3 of its apparent density (Ebbesen,
Thomsen and Mosekilde, 1997), meaning that relatively small
increases in trabecular bone mineral density elicit large increases
in stiffness and strength. In fact, when considering this nonlinear relationship, adaptation to exercise seems to be proportional
in the epiphyses and diaphyses (Wilks et al., 2009a), in keeping
with the view that forces and force-related signals induced by
exercise are proportionate within the different portions of
bones.
Of course, it is important to consider the type of exercise.
Generally exercises involving large muscular forces are found
to be more effective than exercises with low force levels
(Bassey and Ramsdale, 1994; Dickerman, Pertusi and Smith,
2000; Maddalozzo and Snow, 2000; Tsuzuku, Ikegami and
Yabe, 1998; Vincent and Braith, 2002). Accordingly, sprinters
have stronger bones than endurance runners (Bennell et al.,
1997; Wilks et al., 2009a), and weightlifters have particularly
strong bones (Dickerman, Pertusi and Smith, 2000; Karlsson,
Johnell and Obrant, 1993). Moreover, exercises involving
impacts, in particular with unconventional patterns, seem to
have stronger effects upon bone strength than low-impact exercises (Nikander et al., 2005, 2006). This is in line with observations from animal studies of strain rate having an osteogenic
effect per se (Mosley and Lanyon, 1998). Accordingly, alpine
skiers, gymnasts, and ball sports players have enhanced bone
strength. Similarly, vibratory stimuli, as applied through WBV
platforms (Cardinale and Rittweger, 2006), seem to induce bone
accrual (Gilsanz et al., 2006; Gusi, Raimundo and Leal, 2006;
Rubin et al., 2004; Verschueren et al., 2004) independently of
muscular effects (Verschueren et al., 2004).
By contrast, exercises without impact loading seem to be of
little help for bone. Cycling, for example, has traditionally been
c11.indd 140
associated with poor bone health (Medelli et al., 2009; Nichols,
Palmer and Levy, 2003). To support that notion, it is observed
that bone losses occur during the competitive season in cyclists
(Barry and Kohrt, 2008), whilst gymnasts gain bone mass
during the competitive season (Snow et al., 2001). However,
recent studies by Wilks et al. (2009a) and Wilks, Gilliver and
Rittweger (2009b) have demonstrated that the leg bones of track
cyclists are as strong as those of track runners, which may put
the relative importance of impact loading for bone adaptation
into some perspective.
As to the time course of bone adaptive processes, it should
be considered that bone is lost more rapidly than it is accrued.
For example, bone loss starts on the second day of bed rest
(Baecker et al., 2003), but recovery from 2- or 3-month bed rest
occurs only after 12–24 months (Rittweger and Felsenberg,
2009; Rittweger et al., 2010). Accordingly, exercise-induced
gains are readily lost after exercise discontinuation (Winters
and Snow, 2000), although it seems that some long-term benefits in non-exercisers may persist (Kontulainen et al., 1999,
2004).
Although they are not adaptive processes in a strict sense,
we will also discuss here the potential adverse effects that
exercise can have upon tendons and bone.
Fatigue fractures5 occur occasionally in military recruits as
well as in runners and other athletes. It has to be assumed that
repetitive strains promote microdamage generation (see Chapter
1.3), which necessitates bone remodelling.6 Fatigue fractures
occur when the repair process cannot keep up with the rate of
microdamage generation. Often, but not always, pain alerts
against imminent fatigue fractures.
The female athlete triad is a condition characterized by poor
bone status, amenorrhoea and caloric restriction (Otis et al.,
1997). It is frequent in sports where success relies upon leanness, for example in distance running and ballet dancing.
Reduced bone strength is usually caused by oestrogen depletion, which cannot be balanced by the positive osteogenic exercise effects (Bass et al., 1994). Although little is known
regarding the risk of fracture in affected women, the condition
is regarded as potentially dangerous and should receive medical
attention.
2.3.2.4 Bone adaptation across
the life span
We are ignorant as to whether the effects of immobilization
upon bone are modulated across the life span. However, there
is ample evidence to suggest that the relative efficacy of exercise in enhancing bone strength changes as a function of age.
The principles outlined in the last section are based on studies
in adults, and we will now briefly discuss how far these apply
5
Also sometimes misleadingly called ‘stress’ fractures.
This is probably the reason for the reduced cortical bone mineral density in
athletes (by 2% or so, see Haapasalo et al., 2000), which is more pronounced
in endurance runners than in sprinters (Wilks et al., 2009a).
6
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CHAPTER 2.3
ADAPTIVE PROCESSES IN HUMAN BONE AND TENDON
during childhood and puberty, during menopause, and in
old age.
Ample evidence suggests that exercise during childhood
and adolescence increases bone mass and strength (Hughes
et al., 2007; Specker and Binkley, 2003; Witzke and Snow,
2000); most of these studies have focussed on jumping exercises. Although very little is known about other exercises,
one study suggests that resistance training may be more beneficial to bone than hopping during childhood (Morris et al.,
1997). Importantly, the bone’s response to jumping exercises
seems to be enhanced by supplementary calcium intake (Bass
et al., 2007; Specker and Binkley, 2003), underlining the
importance of nutrition. Although little is known about the
effects of puberty in boys, there is clear evidence in girls that
exercise effects are most pronounced during early pubertal
stages (Mackelvie et al., 2001; Matthews et al., 2006; Petit
et al., 2002), and that the efficacy diminishes after menarche
(Bass et al., 1998; Heinonen et al., 2000). Thus, puberty constitutes a window of opportunity in which exercise is most
beneficial toward building strong bones for a life time (Hind
and Burrows, 2007).
The time after menopause is normally associated with bone
losses in the order of 10% (Recker et al., 2000), which are
caused by oestrogen withdrawal (Kalu et al., 1991). Evidence
suggests that exercises may become less effective after menopause (Bassey et al., 1998). However, a number of exercise
intervention studies were able to mitigate (Heinonen et al.,
1998), to prevent (Maddalozzo and Snow, 2000; Milliken et al.,
2003; Rhodes et al., 2000), or even to reverse (Verschueren
et al., 2004) post-menopausal bone losses, showing that the
female skeleton in principle retains responsiveness to physical
stimuli even after menopause.
Old age is often associated with increasing bone losses
(Heaney et al., 2000). However, these losses do not seem to
occur uniformly in the skeleton, but are rather pronounced in
the axial skeleton and the upper extremity, whilst the lower leg
is usually spared (Riggs et al., 2004). Numerous training studies
suggest that the skeleton of older people is susceptible to exercise stimuli, and that positive bone responses can be obtained
(Verschueren et al., 2004; Vincent and Braith, 2002). However,
a recent study in master runners and race-walkers suggests that
osteogenic exercise benefits seem to diminish with increasing
age (Wilks et al., 2009c). Future studies will have to elucidate
whether this is due to decreased responsiveness of bone, or
whether the signals associated with running and other exercises
themselves diminish.
2.3.3
TENDON
2.3.3.1 Functional and
mechanical properties
The primary role of tendons is to transmit contractile forces to
the skeleton in order to generate joint movement. In doing so,
tendons do not behave as rigid bodies, but as springs, and this
has several important functional implications.
c11.indd 141
141
First, having a muscle attached to a compliant tendon makes
it more difficult to control the joint position (Rack and Ross,
1984). Consider, for example, an external oscillating force
applied to a joint at a certain angle: maintaining the joint would
require generation of a constant contractile force in the muscle.
If the tendon of the muscle were very compliant, its length
would change by the external oscillating load, even if the
muscle were held at a constant length. This would result in
failure to maintain the joint at the angle desired. The association
between tendon compliance and joint position control is also
relevant to upright posture. Traditionally, balance of the body
during stance has been considered to be modulated by stretch
reflexes in the calf muscles, such that during forward sway, the
calf muscles are stretched, and the reflex-mediated contraction
plantar flexes the ankle and tilts the body backwards. However,
this requires a very stiff Achilles tendon that can faithfully
convert ankle dorsal flexion to calf-muscle lengthening, and
recent experiments have shown that this does not occur. Instead,
it has been shown that that calf-muscle length change is usually
poorly or negatively correlated with bodily sway, because the
Achilles tendon is compliant relative to the bodily load (for a
review see Loram, Maganaris and Lakie, 2009). This means that
calf-muscle spindles are unable to register bodily sway while
standing, and knowledge of body position is required to appropriately modulate muscle activity and maintain balance.
Second, the elongation of a tendon during a static muscle
contraction is accompanied by an equivalent shortening in the
muscle. For a given contractile force, a more extensible tendon
will allow the muscle to shorten more. This extra shortening
will cause a shortening in the sarcomeres of the muscle. If the
average muscle sarcomere operates in the ascending limb of the
force−length relation, having a more extensible tendon will
result in less contractile force. In contrast, if the average sarcomere operates in the descending limb of the force−length
relation, having a more extensible tendon will result in more
contractile force (Zajac, 1989).
Third, stretching a tendon results in elastic energy storage,
and most of this energy is returned once the tensile load is
removed. This passive mechanism of energy provision operates
in tendons in the feet of legged mammals during terrestrial
locomotion, thus saving metabolic energy that would otherwise
be needed to displace the body ahead (Alexander, 1988).
However, in tendons that stretch and recoil repeatedly under
physiological conditions (e.g. the Achilles tendon), the heat lost
may result in cumulative tendon thermal damage and injury,
predisposing the tendon to ultimately rupture. Indeed, in vivo
measurements and modelling-based calculations during exercise indicate that highly stressed, spring-like tendons may
develop temperature levels above the 42.5 °C threshold for
fibroblast viability (Wilson and Goodship, 1994). These findings are in line with the degenerative lesions often observed in
the core of tendons acting as elastic energy stores, indicating
that hyperthermia may be involved in the pathophysiology of
exercise-induced tendon trauma.
Most of our knowledge of tendon mechanical properties is
based on tests using isolated, non-human material. Two methods
have traditionally been used in biomechanics investigations: (1)
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PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
I
II
III
IV
load cell
clamp
Force
Stiffness
tendon specimen
clamp
displacement
Figure 2.3.4 Schematic illustration of tensile testing apparatus
the free-vibration method, which is based on quantifying the
decay in oscillation amplitude that takes place after a transient
load is applied to a specimen (Ettema, Goh and Forwood,
1998); and (2) tensile testing methodologies, in which the specimen is stretched by an external force, while both the specimen
deformation and the applied force are recorded (e.g. Butler
et al., 1978; Ker, 1992). The latter methodology seems to be
the preferable one in many cases, mostly because it is considered to mimic adequately the way loading is imposed on tendons
in real life.
A tensile testing machine is composed of an oscillating
actuator and a load cell (Figure 2.3.4). The tendon specimen is
gripped by two clamps, a static one mounted on the load cell
and a moving one mounted on the actuator. The actuator is then
set in motion while the load cell records the tension associated
with the stretching applied. The tensile deformation of the
specimen is taken from the displacement of the actuator.
A typical force−deformation plot of an isolated tendon is
shown in Figure 2.3.5. Generally, in force−deformation curves,
slopes relate to stiffness (N/mm), and areas to energy (J). In
elongation-to-failure conditions, four different regions can be
identified in the tendon force−deformation curve. Region I is
the initial concave portion of the curve in which stiffness gradually increases; it is referred to as the tendon ‘toe’ region. Loads
within the ‘toe’ region elongate the tendon by reducing the
crimp angle of the collagen fibres at rest, but they do not cause
further fibre stretching. Hence, loading within the ‘toe’ region
does not exceed the tendon elastic limit; that is, subsequent
unloading restores the tendon initial length. Further elongation
brings the tendon into the ‘linear ’ region II, in which stiffness
remains constant as a function of elongation. In this region,
elongation is the result of stretching imposed in the already
aligned fibres by the load imposed in the preceding ‘toe’ region.
c11.indd 142
Elongation
Figure 2.3.5 Typical force−elongation curve of a tendon pulled by a
load exceeding the tendon elastic limit. I = toe region, II = linear
region, III and IV = failure regions. Stiffness is the slope of the curve
in the linear region
At the end point of this region some fibres start to fail. Thus,
(a) the tendon stiffness begins to drop and (b) unloading from
this point does not restore the tendon initial length. Elongation
beyond the ‘linear ’ region brings the tendon into region III,
where additional fibre failure occurs in an unpredictable way.
Further elongation brings the tendon into region IV, where
complete failure occurs.
Although regions I, II, III, and IV are apparent in tendon
force−deformation curves during elongation-to-failure conditions, the shapes of the curves obtained differ between specimens. To a great extent these differences can be accounted
for by inter-specimen dimensional differences. For example,
tendons of equal length but different cross-sectional area
exhibit different force−deformation properties; thicker tendons
are stiffer. Similarly, different force−deformation curves are
obtained from tendons of equal cross-sectional area but different initial length; shorter tendons are stiffer (see Butler
et al., 1978). To account for inter-specimen dimensional differences, tendon force is reduced to stress (MPa) by normalization to the tendon cross-sectional area, and tendon
deformation is reduced to strain (%) by normalization to the
tendon original length. The tendon stress−strain curve is similar
in shape to the force−deformation curve, but reflects the
intrinsic material properties rather than the structural properties of the specimen.
The most common material parameters taken from a
stress−strain curve under elongation-to-failure conditions are
the Young’s modulus (GPa), the ultimate stress (MPa), and the
ultimate strain (%). The Young’s modulus is calculated as the
product of the stiffness and the original length-to-cross-sectional
area ratio of the specimen. Experiments on several tendons
indicate that the Young’s modulus reaches the level of 1–2 GPa
at stresses exceeding 30 MPa, the ultimate tendon stress (i.e.
stress at failure) ranges from 50 to 100 MPa, and the ultimate
tendon strain (i.e. strain at failure) ranges from 4 to 10%
(Bennett et al., 1986; Butler et al., 1978; Pollock and Shadwick,
1994).
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CHAPTER 2.3
2.3.3.2
ADAPTIVE PROCESSES IN HUMAN BONE AND TENDON
In vivo testing
The examination of human tendon properties under in vitro
conditions necessitates the use of donor specimens, which are
not always readily available. Moreover, caution should be
adopted when using the results of the in vitro test to infer in
vivo function for the following reasons: (1) the forces exerted
by maximal tendon loading under in vivo conditions may not
reach the ‘linear ’ region where stiffness and Young’s modulus
are measured under in vitro conditions; (2) clamping of an
excised specimen in a testing rig is inevitably associated with
some collagen fibre slippage and stress concentration that may
result in premature rupture (Ker, 1992); (3) in vitro experiments
have often been performed using preserved tendons, which may
have altered properties (Matthews and Ellis, 1968; Smith,
Young and Kearney, 1996).
Recently, however, a non-invasive method for assessing the
mechanical properties of human tendons in vivo that circumvents the above problems was developed. This method is based
on ultrasound scanning of a reference point along the tendon
during an isometric contraction (Maganaris and Paul, 1999).
The muscle forces generated by activation are measurable by
dynamometry. They pull the tendon, causing a longitudinal
deformation that can be quantified by measuring the displacement of the reference landmark on the scans recorded (Figure
2.3.6). The force–elongation plots obtained during loading–
unloading can be transformed to the respective stress–strain
plots by normalization to the dimensions of the tendon, which
can also be measured using non-invasive imaging.
2.3.3.3 Tendon adaptations to altered
mechanical loading
The general principles of in vivo tendon testing have often been
applied to the study of the adaptations of human tendon to
altered mechanical loading. The effect of increased or decreased
chronic mechanical loading on the mechanical properties of
human tendons in vivo has been examined in a number of crosssectional and longitudinal design studies.
Cross-sectional studies
Cross-sectional studies have mainly compared (1) highlystressed versus low-stressed tendons in a given sample, (2)
tendons in sedentary versus athletic populations, (3) healthy
versus disused tendons and (4) tendons in different age groups.
1. Tendons subjected to different habitual loading: when comparing the human Achilles/gastrocnemius and tibialis anterior tendons of young adults using the same methodology, it
emerges that these two tendons have very similar Young’s
modulus (1.2 GPa) (Maganaris, 2002; Maganaris and Paul,
1999, 2002). This finding should be interpreted bearing in
mind that the gastrocnemius and tibialis anterior tendons are
subjected to different physiological forces. The gastrocnemius tendon is subjected to the high forces generated in late
c11.indd 143
143
TA tendon
A
B
C
D
E
F
G
1 cm
distal end
proximal end
Figure 2.3.6 Typical in vivo sonographs of the human
tibialis anterior (TA) tendon. A = resting state, B = 40% of
maximal isometric contraction during activation, C = 80%
of maximal isometric contraction during activation, D = 100%
of maximal isometric contraction, E = 80% of maximal
isometric contraction during relaxation, F = 40% of maximal
isometric contraction during relaxation, G = 0% of maximal isometric
contraction at the end of relaxation. The white arrow in each scan
points to the TA tendon origin. The black double arrows point to the
shadow generated by an echo-absorptive marker glued on the skin to
identify any displacements of the scanning probe during muscle
contraction–relaxation. The tendon origin displacement is larger
during relaxation than with contraction at each loading level,
indicating the presence of mechanical hysteresis in the tendon.
Reproduced, with permission, from Maganaris, C. N. & Paul, J. P.,
2000. ‘Hysteresis Measurements in Intact Human Tendon’. J.
Biomechanics. 33:12 © Elsevier
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stance and the tibialis anterior tendon is subjected to the
lower forces generated by controlling ankle plantar flexion
in the early stance phase of gait. In vivo measurements of
tendon force indicate that the Achilles tendon may carry up
to 110 MPa in each stride during running (Komi, Fukashiro
and Jarvinen, 1992). This stress exceeds the average ultimate
tensile tendon stress of 100 MPa (Butler et al., 1978; Bennett
et al., 1986), which highlights the possibility of Achilles
tendon rupture in a single pull in real life. Epidemiological
studies of spontaneous tendon rupture verify these theoretical considerations (Jozsa and Kannus, 1997). Notwithstanding
the above stress difference between the two tendons, the
gastrocnemius tendon was not found to be intrinsically
stiffer than the tibialis anterior tendon, which agrees with
previous findings on several isolated animal tendons (Pike,
Ker and Alexander, 2000; Pollock and Shadwick, 1994).
Consistent with this result is the finding of Couppé et al.
(2008) of increased patellar tendon cross-sectional area and
stiffness, but not Young’s modulus, in the stronger leg compared to the weaker leg of elite athletes. These findings
indicate that adjustments in tendon structural properties to
differences in habitual loading are accomplished by adding
or removing material so that the tendon becomes thicker or
thinner, rather than altering the intrinsic material properties.
This notion is consistent with a theory developed by Ker,
Alexander and Bennett (1988), according to which the thickness of the tendon is determined by the criterion of minimal
combined mass for the tendon and its muscle, and the
muscle-to-tendon-area ratio is rather constant. Crosssectional data on humans (An, Linscheid and Brand, 1991)
support the theory of Ker, Alexander and Bennett (1988),
but recent results from longitudinal, interventional studies,
which will be discussed below, challenge it and indicate that
alterations in tendon size may not always be the sole mechanism underlying tendon stiffness adaptations to loading.
2. Tendons in sedentary versus athletic populations: The results
of such comparative studies are insightful, but it should be
considered that they may be confounded by self-selection
bias and inter-subject variability in exercise training history.
In one study, the cross-sectional area of the Achilles
tendon has been shown to be greater along its length in longdistance runners than controls (Magnusson and Kjaer, 2003),
with greater differences in the distal region of the tendon,
close to the calcaneal attachment, suggesting that sitespecific tendon hypertrophy may be associated with compressive rather than tensile tendon loading. Despite the
differences in tendon size between the two groups and
the reduced tendon stress in the runners, the stiffness of the
Achilles tendon-aponeurosis was similar in runners and nonrunners (Rosager et al., 2002). A similar finding was reported
by Arampatzis et al. (2007a), who included three subject
groups in their study: endurance runners, sprinters, and controls. The stiffness of the Achilles tendon-aponeurosis was
greater in the sprinters than in controls, but there were no
differences between endurance runners and non-runners and
there was a significant correlation between tendon stiffness
and tendon force during maximum voluntary contraction.
c11.indd 144
However, Kubo et al. (2000a) reported no differences in the
Achilles tendon-aponeurosis stiffness between sprinters and
controls. Taken together, the above data suggest that the
Achilles tendon-aponeurosis stiffness does not show a
response proportional to the intensity of the physical activity
performed and there may be a threshold, corresponding to
the intensity/frequency/volume of training, above which
mechanical stimuli can evoke adaptive responses. In contrast
to the Achilles tendon-aponeurosis, the quadriceps femoris
tendon-aponeurosis in endurance runners has been shown to
be stiffer than in controls (Kubo et al., 2000b), indicating
that the threshold value for adaptation in this tendonaponeurosis may be lower than in the Achilles tendonaponeurosis. In a study on tendon stiffness in relation to
running economy (Arampatzis et al., 2006) it was found that
the most economical runners had lower quadriceps tendonaponeurosis stiffness at low tendon forces, resulting in
higher strains and a greater elastic energy storage and
release, which could reduce the metabolic cost of running.
A lower quadriceps tendon-aponeurosis stiffness was also
reported for faster sprinters compared to slower sprinters and
a correlation was found between the maximum tendonaponeurosis strain and the 100 m time (Stafilidis and
Arampatzis, 2007), suggesting greater energy storage and
recovery, and faster contractile shortening in the faster
sprinters.
3. Healthy versus disused tendons: in cross-sectional studies,
pathology-induced immobilization has been used as a model
of disuse. One study compared the mechanical properties of
the patellar tendon in able-bodied men and SCI men, with
durations of lesion ranging from 1.5 to 24 years (Maganaris
et al., 2006). It was found that the tendons of the SCI subjects had a reduced stiffness of 77% and a reduced Young’s
modulus of 59% compared with the able-bodied subjects
(Figure 2.3.7). The reduced Young’s modulus with SCI indicates that chronic disuse deteriorates the material of the
tendon. However, the tendons of the SCI subjects also had
smaller cross-sectional areas (by 17%, Figure 2.3.8), indicating that they may have undergone atrophy. The possibility
that some of the differences in tendon cross-sectional area
between the two subject groups relate to their anthropometric characteristics rather than atrophy cannot be excluded,
although it should be noted that the length of the tendons
was similar in the two groups. No apparent relation was
observed between the deterioration of tendon and the duration of lesion, indicating that most of the deterioration of
tendon occurred rapidly, within the first few months of
immobilization. However, a proper longitudinal study with
measurements at different time points after the lesion would
be required to shed more light on the dose–response relation
of adaptations in human tendon with immobilization.
In a more recent study, the mechanical properties of the
human patellar tendon were examined in individuals who
had undergone surgical reconstruction of the anterior cruciate ligament using a patellar tendon graft between 1 and 10
years before the study (Reeves et al., 2009). Cross-sectional
area of the operated patellar tendons was 21% larger than
10/18/2010 5:11:32 PM
CHAPTER 2.3
A
ADAPTIVE PROCESSES IN HUMAN BONE AND TENDON
145
4000
able-bodied
3500
SCI
AB
Force (N)
3000
2500
2000
SCI
1500
1000
10 mm
500
0
0
B
2
4
Elongation (mm)
6
35
able-bodied
30
SCI
Stress (MPa)
25
20
15
10
5
0
0
5
10
Strain (%)
15
Figure 2.3.7 Patellar tendon (a) force–elongation and(b) stress–stain
data for able-bodied (AB) and spinal cord-injured (SCI) subjects.
Data are means and SD (n = 6 per group). Reproduced, with
permission, from Maganaris, C. N., Reeves, N. D., Rittweger, J. et al.
2005. ‘Adaptive Response of Human Tendon to Paralysis’ in ‘Muscle
and Nerve’ © John Wiley & Sons
the contralateral, control tendons. Although the Young’s
modulus was 24% lower in the operated tendons, the operated and control tendons had similar stiffness values. It
seems that a compensatory enlargement of the patellar
tendon, presumably due to scar-tissue formation, enabled a
recovery of tendon stiffness in the operated tendons.
4. Tendons in different age groups: maturation and ageing are
two contrasting biological processes which involve altered
mechanical loading for the tendon and for the whole muscu-
c11.indd 145
Figure 2.3.8 Axial-plane ultrasounds showing the cross-sectional
area of the patellar tendon in its mid-region in an able-bodied (AB)
subject (tendon length = 38 mm) and a spinal cord-injured (SCI)
subject (tendon length = 46 mm). Reproduced, with permission, from
Maganaris, C. N., Reeves, N. D., Rittweger, J. et al. 2005. ‘Adaptive
Response of Human Tendon to Paralysis’ in ‘Muscle and Nerve’ ©
John Wiley & Sons
loskeletal system. This is because in pre-pubertal age the
muscle forces that are exerted in order to support the smaller
mass of the human body are also smaller, and older individuals are generally more sedentary than younger individuals.
This factor alone could reduce the tendon mechanical properties in both pre-pubescence and old age compared with
adolescence. Indeed, studies have shown that there is an
increase in the stiffness (Kubo et al., 2001a) and Young’s
modulus (O’Brien et al., 2010) of tendons in adolescents
compared with pre-pubertal children, whereas ageing has
been shown to gradually deteriorate the tendon’s mechanical
properties (Karamanidis and Arampatzis, 2005; Onambele,
Narici and Maganaris, 2006). However, it should be emphasized that there are age-driven processes taking place that
affect the mechanical behaviour of the tendons independent
of the loading conditions present; for example, in ageing
there is an increase in collagen cross-linking, which increases
the stiffness of the tendon (Kjaer, 2004). However, in one
recent study there were no differences in the patellar tendon
Young’s modulus between younger and older individuals,
despite the increased collagen cross-linking in the older
group (Couppé et al., 2009). This inter-study discrepancy
may reflect lifestyle differences between the older individuals examined.
Longitudinal studies
Longitudinal studies have made pre- versus post-intervention
comparisons where chronic loading has been manipulated by
introducing exercise training or disuse.
1. Exercise training: most training studies have employed
resistance exercise for several weeks in order to chronically
overload the tendons of the exercised muscles.
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Kubo et al. (2001b) examined the effects of isometric
knee extensor muscle strength training for 12 weeks, four
times a week, and found an increase in the stiffness of the
quadriceps tendon-aponeurosis after training. No measurements of tendon size were taken, so it is not known whether
the stiffness change was attributable to changes in tendon
cross-sectional area and/or Young’s modulus. Reeves,
Maganaris and Narici (2003) examined the effects of
dynamic knee extensor muscle strengthening for 14 weeks,
three times a week, in older individuals, and found an
increase in both patellar tendon stiffness and Young’s
modulus, but not in tendon cross-sectional area. It was concluded that the stiffness increase was caused solely by
changes in the material of the tendon and not by tendon
hypertrophy. Three recent studies, however, challenge this
finding. Kongsgaard et al. (2007), Arampatzis, Karamanidis
and Albracht (2007b), and Seynnes et al. (2009) all showed
that there was regional tendon hypertrophy in response to
resistance training between 9 and 14 weeks, indicating that
in the earlier study of Reeves, Maganaris and Narici (2003)
some regional tendon hypertrophy may actually have
occurred but gone undetected due to the limited number
of scans (three) recorded along the tendon. In contrast
to Reeves, Maganaris and Narici (2003), Arampatzis,
Karamanidis and Albracht (2007b), and Seynnes et al.
(2009), it must be noted that Kongsgaard et al. (2007)
reported no improvement in the tendon Young’s modulus
after training. However, it should also be noted that in the
latter study the smallest tendon cross-sectional area was used
in the calculation of tendon stress, while the former three
studies used mean values. In the studies of Kubo et al.
(2001b), Kongsgaard et al. (2007), and Arampatzis,
Karamanidis and Albracht (2007b)), the contralateral leg
was also trained. Kubo et al. used smaller durations of
loading per repetition, Kongsgaard et al. used smaller resistance during contraction and therefore smaller tendon strains,
and Arampatzis et al. used directly smaller tendon strains.
In all three studies, the volume of training was the same for
the two legs. However, the properties of tendon did not
change in the legs trained using the lighter stimuli, indicating
that there is a threshold above which mechanical loading can
induce tendon hypertrophy and/or improvement in Young’s
modulus.
Studies have also examined the effects of stretching on
tendon properties to investigate whether the resultant
increases in joint range of movement and reduction in joint
stiffness are associated with changes in tendon properties.
Kubo, Kanehisa and Fukunaga (2002) applied ankle stretching for three weeks and found that there was no change in
Achilles tendon stiffness. Similarly, Morse et al. (2008)
found no changes in Achilles tendon stiffness after acute
passive ankle stretches, and the measurements taken showed
that the increased whole-muscle tendon length due to the
greater joint range of movement post-stretching was attributed to an extension of the muscle belly, which became more
compliant. However, the changes in muscle fascicle length
corrected for the effect of pennation could not account for
c11.indd 146
the extension of the muscle belly, indicating lengthening of
the muscle’s aponeuroses, rather than muscle extension by
pivoting of the muscle fascicles around their insertion points
in the aponeuroses alone.
2. Disuse: longitudinal studies have examined the effects of
disuse, induced by means of immobilization and bed rest.
In a unilateral limb-suspension study, the patellar tendon
of the unloaded leg of the participants was tested at base line
and after 14 and 23 days of suspension. There was no change
in the tendon’s dimensions, but there was a gradual decrease
in the tendon stiffness and Young’s modulus, by about 10%
and 30% on days 14 and 23 of the intervention respectively.
The rate of tendon collagen synthesis, assessed by quantifying the incorporation of non-radioactive isotopes in tendon
tissue samples obtained by biopsy, also fell gradually during
the intervention, with most of the reduction occurring in the
first 10 days. The above results indicate that the reduction
in protein synthesis could be associated with a reduced collagen fibril density, rather than with atrophy at a wholetendon level. In contrast to these findings, Christensen et al.
(2008a) showed no changes in Achilles tendon collagen
synthesis after two weeks of plaster-induced immobilization,
by using microdialysis to detect markers of collagen synthesis in the peritendinous area. This discrepancy may indicate
that: (i) the microdialysis and isotope tracing techniques do
not have the same sensitivity; (ii) there is a difference in the
level of disuse between the limb-suspension and plaster
models for equal durations of application of the two interventions; (iii) different tendons require different durations/
levels of disuse before their collagen synthesis starts to drop,
depending on the habitual use and loading of the tendon.
Somewhat surprising is the finding of Christensen et al.
(2008b), who used the micodialysis technique and showed
that seven weeks of plaster-induced immobilization, not for
experimental purposes but for the treatment of unilateral
ankle fractures, increased tendon collagen synthesis and
degradation, while a remobilization period of similar length
reduced collagen synthesis and degradation to baseline
levels. However, it is possible that the ankle fracture close
to the tendon sampling site affected the above data. There
was no change in the Achilles tendon cross-sectional area
throughout the entire study.
The results of bed-rest studies show substantial deterioration of tendon properties with disuse. Kubo et al. (2004)
examined the quadriceps tendon-aponeurosis before and
after 20 days of bed rest, and Reeves et al. (2005) examined
the gastrocnemius tendon before and after 90 days of bed
rest. In both studies there was a substantial reduction in
tendon stiffness after bed rest. No tendon dimensions were
measured in the former study, but in the latter there was no
significant change in the tendon’s cross-sectional area after
bed rest and therefore the tendon stiffness reduction could
almost entirely be attributed to deterioration in the tendon’s
material. However, as stated earlier, the possibility of some
regional tendon atrophy going undetected due to the limited
scans recorded cannot be excluded. The assessment of
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CHAPTER 2.3
ADAPTIVE PROCESSES IN HUMAN BONE AND TENDON
Figure 2.3.9 Tendon stress–stain data before and after 90 days of
bed rest (preBR and postBR, respectively) and before and after bed
rest plus exercise (preBREx and postBREx, respectively). Exercise
partly attenuates the deteriorating effect of disuse. Data are means
(n = 9 per group). Reproduced, with permission, from Reeves, N. D.,
Maganaris, C. N., Ferretti, G. and Narici, M. V. 2005. ‘Influence of
90-day simulated microgravity on human tendon mechanical
properties and the effect of resistive countermeasures’. J. Appl.
Physiol. 98: 2278–2286. © Americal Physiological Society
tendon properties in the study of Reeves et al. (2005) was
carried out using the same methodology and analysis as in
the SCI study by Maganaris et al. (2006), and the deteriorations in tendon stiffness and Young’s modulus were of
similar magnitude, despite the two studies employing different durations of mechanical unloading: 90 days in the bedrest study and up to 24 years of paralysis in the SCI study.
This is consistent with the notion that that most of the deterioration of tendon during chronic disuse occurs rapidly,
within the first few months. In the studies of both Kubo
et al. (2004) and Reeves et al. (2005) there was an additional
subject group, which underwent resistance exercise throughout the bed-rest period, and in both studies the addition of
exercise attenuated, at least partly the deteriorating effect of
disuse (Figure 2.3.9). This indicates that any exercises
undertaken to strengthen and condition the skeletal muscles
during prolonged periods of clinical disuse, for example
confinement to a hospital bed, may also be beneficial for the
tendons.
2.3.4
CONCLUSION
In conclusion, there is clear evidence that exercise has positive
effects upon bone, leading to denser trabecular networks,
c11.indd 147
147
greater cortical thickness, and thus an enhancement of wholebone strength. These effects are most likely mechanically mediated, as they are site-specific, reversible, and strongest when the
exercise involves large forces and impacts. Moreover, the
effects are most pronounced during puberty, and they seem to
diminish with increasing age.
However, despite the fact that exercise effects upon bone
are beneficial, they are quite small and do not usually exceed
3% in interventional studies. Differences between athletes and
sedentary people can amount to up to 20%, but this is probably
partly due to self-selection bias (Wilks et al., 2009a). Therefore,
osteogenic exercise effects are small when compared to the
rapid bone accrual in the early stages after bed rest (Figure
2.3.3a). The important question therefore arises as to what
limits further accrual of bone mass, both in exercise and after
bed rest (Figure 2.3.3b). In consideration of the enormous
potential to recover lost bone (Rittweger and Felsenberg, 2009),
it seems that this limitation is not imposed by bone itself.
Rather, the soft tissues defining the mechanical interfaces to
bone, such as tendinous structures (Rittweger et al., 2005b) and
effective joint size (Rittweger, 2008), are more likely to set
effective limits to bone accrual.
Similar to bones, tendons deteriorate in response to mechanical unloading, and this is at least partly explained by an inferior
tendon material as a whole. Unlike bones, however, tendons do
show substantial positive adaptations and increase their
mechanical stiffness in response to chronic exercise, as shown
by a number of interventional and cross-sectional studies.
Furthermore, we now understand a lot more about the mechanisms mediating the conversion of mechanical loading to biochemical changes that lead to tendon stiffness improvements.
Using the microdialysis technique it has been shown that the
rate of tendon collagen synthesis increases very rapidly in
response to exercise, within six hours after a single bout of
exercise, and by twice as much as at rest 24 hours post-exercise
(Miller et al., 2005). We also know that net collagen synthesis
in the tendon increases in response to exercise training, and that
this is associated with a dominance of collagen synthesis over
degradation (Langberg, Rosendal and Kjaer, 2001). Collagen
degradation is mediated by activation of matrix metaloproteinases (MMPs), while synthesis is mediated by over-expression
of growth factors, such as TGF-a, IL-6, and IGF-I, some of
which may also reduce collagen degradation by suppressing
MMPs and stimulating their inhibitors (TIMPs) (Heinemeier
et al., 2003; Koskinen et al., 2004; Kjaer, 2004; Langberg
et al., 2002; Olesen et al., 2007). Interestingly, oral-contraceptive
users have suppressed IGF-I and rate of tendon collagen synthesis after a single bout of exercise (Hansen et al., 2008), and
it remains to be investigated whether a similar effect occurs
after long-term training, which may provide clues to the incidence of certain gender-related sports injuries. At a wholetendon level, in vivo studies show that the adaptations to
increased mechanical loading vary, and may include (1) regional
increases in tendon cross-sectional area without changes in the
tendon’s material, (2) improvement in the tendon’s material
without any changes in its dimensions, or (3) changes in both
material and cross-sectional area of the tendon.
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But why are there size increases in some and not all, or in
none of the tendon regions? Is the answer simply that the
current in vivo imaging techniques do not have the sensitivity
to allow the measurement of small tendon size changes, or is
this a true effect, related, for example, to the anatomical location and biomechanical environment of the tendon? If the latter
is the case, what is the molecular basis underlying the differen-
c11.indd 148
tiation of tendon hypertrophy from a qualitative tendon change
unrelated to the tendon’s size? Addressing these important
questions will allow us to unravel the mechanisms regulating
tendon plasticity and help us optimize the effectiveness of exercise interventions for ‘tendon strengthening’ in different tendons
and individuals according to specific needs, such as sporting
competition and rehabilitation after injury.
10/18/2010 5:11:32 PM
CHAPTER 2.3
ADAPTIVE PROCESSES IN HUMAN BONE AND TENDON
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2.4 Biochemical Markers and
Resistance Training
Christian Cook1,2,3 and Blair Crewther3, 1 United Kingdom Sport Council, London, UK, 2 University of Bath, Sport,
Health and Exercise Science, Bath, UK, 3 Imperial College, Institute of Biomedical Engineering, London, UK
2.4.1
INTRODUCTION
2.4.2
The mechanical and hormonal responses to resistance training
or weight training have been proposed as necessary stimuli for
training adaptations to occur (Crewther et al., 2006; Häkkinen,
1989; Kraemer, 2000; Kraemer and Mazzetti, 2003). In particular, hormones play an important role in the resistance training
process by regulating protein turnover and long-term changes
in skeletal muscle growth. Since the cross-sectional area (CSA)
of muscle is also a determinant of muscle force production
(Bruce, Phillips and Woledge, 1997), the long-term effects of
hormones upon muscle CSA can also influence both power and
strength adaptation. Perhaps the most widely examined steroid
hormones from this perspective are testosterone (T) and cortisol
(C), often considered the primary anabolic and catabolic
hormones, respectively, along with the polypeptide growth
hormone (GH) (Crewther et al., 2006; Häkkinen, 1989;
Kraemer, 2000; Kraemer and Mazzetti, 2003).
Resistance training is known to stimulate acute changes in
blood hormone concentrations, which are thought to mediate
those cellular processors involved in muscle growth (Kraemer,
2000; Kraemer and Mazzetti, 2003). Thus, the design of individual workouts (e.g. load, volume, rest periods, etc.) plays an
important role in mediating long-term adaptation with training.
With this in mind, examining the acute responses of the aforementioned hormones to different workouts (e.g. hypertrophy,
strength, explosive power) would provide a better understanding of how various training methods affect the hormonal milieu
and hypertrophy, power, and strength adaptation thereafter.
Discussion of the additional effects of age, gender, and training
history would add to this analysis. Although this review will
focus primarily on T, C, and GH, this in no way suggests the
primacy of these three examples, but it does allow for a more
detailed discussion of their relevance to the resistance training
process.
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
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TESTOSTERONE RESPONSES TO
RESISTANCE TRAINING
The free or biologically active form of T accounts for ∼1–2%
of all T, with ∼38–50% bound to albumin and the remaining
portion bound to sex hormone-binding globulin (Dunn, Nisula
and Rodbard, 1981; Loebel and Kraemer, 1998). The T portion
bound to albumin is believed to be readily available for metabolism, due to enhanced dissociation (Pardridge, 1986),
effectively contributing to the bioavailable hormone pool. The
majority of evidence supports T as having an important anabolic effect upon muscle tissue growth (Crewther et al., 2006;
Herbst and Bhasin, 2004). In this role, T is thought to contribute
directly to muscle protein synthesis, whilst also reducing muscle
protein degradation (Herbst and Bhasin, 2004). Indirectly, T
may also stimulate the release of other anabolic hormones (e.g.
GH) important for muscle tissue growth (Crewther et al., 2006).
2.4.2.1
Effects of workout design
Hypertrophy workouts generally result in large increases in T
concentrations, whilst maximal strength workouts elicit much
smaller or no hormonal changes, measured in blood or saliva
(Consitt, Copeland and Tremblay, 2001; Crewther et al., 2008;
Gotshalk et al., 1997; Häkkinen and Pakarinen, 1993; Kraemer
et al., 1991; Linnamo et al., 2005; McCaulley et al., 2009;
Smilios et al., 2003). For instance, a 72% increase in T concentrations was noted after a hypertrophy session (10 repetition
maximum (RM) load, high volume, 1 min rest periods) in men,
whilst a maximal strength session (5 RM, moderate volume, 3
min rest periods) elevated T by only 27% in the same group
(Kraemer et al., 1991). Explosive power workouts (<50% 1
RM, low–moderate volume, 1–3 min rest periods) can also
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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acutely increase T concentrations (Mero et al., 1991; Volek
et al., 1997), although not to the same extent as those training
sessions designed to increase muscle size. On the other hand,
other studies have reported no changes in the acute T responses
to explosive training protocols (Crewther et al., 2008; Linnamo
et al., 2005; McCaulley et al., 2009).
2.4.2.2
Effects of age and gender
Age is one factor influencing the acute hormonal responses to
resistance exercise. Resistance exercise is known to increase T
concentrations among younger males (Fry et al., 1993; Kraemer
et al., 1992; Mero et al., 1993), but to a much lower extent than
in their older male counterparts (Mero et al., 1993; Pullinen
et al., 2002). Resting T concentrations are also much greater in
adult males (Mero et al., 1993; Pullinen et al., 2002). These
differences are likely to provide adult males with a more beneficial response for adaptation and thereby explain muscle mass
and strength differences between adult and younger males. The
acute T responses to resistance exercise decrease in later life,
as do basal concentrations of T (Häkkinen and Pakarinen, 1995;
Kraemer et al., 1998a, 1999). These changes in androgen activity may partly explain the reduction in muscle mass and strength
seen with increasing age. Proposed mechanisms include failure
of the hypothalamic-pituitary axis, changes in testicular function, an increase in SHBG levels, and/or increased sensitivity
of gonadotropin secretion to androgen negative-feedback inhibition (Vermeulen, Rubens and Verdonck, 1972).
Gender also plays a role in modulating the hormonal
responses, with resistance training sessions found to produce
reliable T increases in males, but no T changes noted in females
performing the same workouts (Kraemer et al., 1991; Linnamo
et al., 2005). Possibly this relates to different mechanisms of
secretion, with males producing much greater androgen concentrations overall, as well as larger acute responses via the testes.
However, a broad range of protocols have not been explored
and females have shown elevated T across different modes of
exercise (Consitt, Copeland and Tremblay, 2001; Copeland,
Consitt and Tremblay, 2002). The differential response patterns
between males and females, along with the greater (5–10-fold)
basal concentrations of T in males (Kraemer et al., 1991;
Linnamo et al., 2005), support the general observation that men
exhibit greater muscle mass and strength than females, as well
as having a greater training capacity for inducing changes in
these variables.
2.4.2.3
Effects of training history
Training history can also influence the acute hormonal
responses. Resistance-trained athletes were found to produce a
greater T response than endurance athletes (Tremblay, Copeland
and Van Helder, 2004) and non-athletes (Ahtiainen et al.,
2004). Likewise, a nine-week training period markedly
increased the acute T response in men (Kraemer et al., 1998b),
with other evidence showing that greater training experience is
c12.indd 156
accompanied by greater T responses to resistance exercise
(Kraemer et al., 1988, 1992). Training can also affect resting
hormones; for instance male sprinters have higher resting T
than soccer players, who in turn have higher T than crosscountry skiers (Bosco and Viru, 1998), while sprinters have
higher T than handball players (Cardinale and Stone, 2006).
Conversely, the T concentrations of endurance athletes were
found to be less than more explosive athletes and/or sedentary
or active controls (Grasso et al., 1997; Hackney, Fahrner and
Gulledge, 1998, Hackney, Szczepanowska and Viru, 2003;
Izquierdo et al., 2004). These T differences might be functionally important in meeting the force demands of athletes during
exercise, training, and competition; alternatively, these findings
could represent genetic predisposition and the natural selection
of participants towards different sports.
2.4.3 CORTISOL RESPONSES TO
RESISTANCE TRAINING
Most C is bound to plasma proteins in blood, with ∼80% bound
to corticosteroid-binding globulin and ∼6% to albumin (Dunn,
Nisula and Rodbard, 1981). Approximately 1–5% of C circulates freely and is biologically active, although the saturation of
corticosteroid-binding globulin can also lead to dramatic
increases in the free moiety (Dunn, Nisula and Rodbard, 1981;
Rowbottom et al., 1995). Traditionally, C has been regarded as
the primary catabolic hormone, as it decreases protein synthesis
and increases the breakdown of muscle protein (Crewther et al.,
2006; Viru and Viru, 2004). Likewise the anti-anabolic properties of C are linked to the attenuation of other anabolic hormones such as T and GH (Crewther et al., 2006). However, a
more correct interpretation may be to view acute changes in C
as a prerequisite for the repartitioning of metabolic resources;
an essential step in hypertrophy (Viru and Viru, 2004).
2.4.3.1 Effects of workout design
Most research concludes that hypertrophy workouts elicit a
greater acute C response than maximal-strength workouts
(Crewther et al., 2008; Häkkinen and Pakarinen, 1993; Kraemer
et al., 1993; McCauley et al., 2009; Smilios et al., 2003;
Zafeiridis et al., 2003). Kraemer et al. (1993) reported a 125%
increase in female C concentrations after a hypertrophy workout,
but no hormonal changes were noted following a maximalstrength workout. Similarly, workouts designed to improve
explosive power generally do not alter C concentrations
(Crewther et al., 2008; Linnamo et al., 2005; McCaulley et al.,
2009; Mero et al., 1991). The results of some studies have suggested that C concentrations may even decline across certain
forms of resistance training (Beaven, Gill and Cook, 2008a;
Crewther et al., 2008; Smilios et al., 2003). Theoretically, if the
testosterone-to-cortisol ratio (T/C) is important, as some
suggest, then the use of the T/C may be advantageous to
evaluate the net hormonal effects imposed by different training
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workouts. However, sampling differences, the study population, and training status all need careful consideration when
comparing studies.
2.4.3.2
Effects of age and gender
The acute C response to resistance exercise was found to be
much greater in younger males than in adult males (Mero
et al., 1993; Pullinen et al., 2002). In their study, Pullinen
et al. (2002) compared the hormonal responses of men, women,
and pubescent boys to a single exercise bout (5 sets x 10 knee
extensions, 40% 1 RM) followed by two sets to exhaustion.
Only the boys revealed an acute increase in C concentrations.
Furthermore, peak epinephrine concentrations (another stress
hormone) were found to be twice as high in this group, as
compared to men and women. These data are indicative of a
greater stress response among younger males. Differences in
maturation, anxiety and adaptive capability to resistance exercise may be important factors in this respect (Pullinen et al.,
2002). Once adulthood has been reached, however, age appears
to have little or no effect upon the acute C responses to a bout
of resistance exercise (Häkkinen and Pakarinen, 1995; Kraemer
et al., 1999).
The responsiveness of C to resistance exercise appears to be
similar between males and females, regardless of the type of
workout performed (Häkkinen and Pakarinen, 1995; Kostka
et al., 2003; McGuigan, Egan and Foster, 2004; Pullinen et al.,
2002). Kraemer et al., 1998b also found no significant differences in the acute C responses of males and females to a single
exercise bout, performed before and after an eight-week period
of heavy-resistance training. Subsequently, the stimulus of
resistance exercise would seem to elicit similar adrenal stress
responses for both males and females. The resting concentrations of C are also largely similar for males and females
(Häkkinen and Pakarinen, 1995; Kostka et al., 2003; McGuigan,
Egan and Foster, 2004; Pullinen et al., 2002). Given these findings, it may be speculated that gender differences in muscle
mass and performance are primarily driven by the differential
response patterns of the anabolic hormones.
2.4.3.3
Effects of training history
The effects of training history upon C secretory patterns are less
clear. A similar C response was reported by resistance-trained
(380%) and sedentary males (380%), although the loads utilized
were vastly different (Tremblay, Copeland and Van Helder,
2004). Other research has reported either small or no changes
in the acute C responses after periods of weight training
(Kraemer et al., 1998b; McCall et al., 1999), or demonstrated
that training experience does not influence these responses
(Ahtiainen et al., 2004; Kraemer et al., 1992). However, one
study reported a greater C response in untrained individuals
following resistance exercise, compared to that seen in trained
individuals (McMillan et al., 1993), the possible result of
greater perception of stress among those with no training expe-
c12.indd 157
157
rience, even though they exercised at the same relative load
(McMillan et al., 1993). In contrast to T, basal C concentrations
were found to be no different between various athletic groups
and controls (Ahtiainen et al., 2004; Grasso et al., 1997;
Hackney, Fahrner and Gulledge, 1998; Izquierdo et al., 2004).
2.4.4 DUAL ACTIONS OF
TESTOSTERONE AND CORTISOL
T and C appear to have dual actions upon the neuromuscular
system: first, acting in the traditional longer time frame through
a genomic pathway; and second, acting on a much shorter time
frame through a non-genomic pathway. As supporting evidence, both T and C have been shown to induce rapid (i.e.
seconds to minutes) changes in neuronal activity within the
animal brain (Chen et al., 1991; Jansen et al., 1993; Smith,
Jones and Wilson, 2002; Zaki and Barrett-Jolley, 2002). These
steroid hormones can also produce relatively rapid changes in
mood, behaviour, and/or cognitive function in animals (Aikey
et al., 2002; James and Nyby, 2002; Schiml and Rissman, 1999)
and humans (Aleman et al., 2004; Hermans et al., 2006; Hsu
et al., 2003). In addition, these hormones can both produce
rapid changes in intracellular Ca2+ in muscle cells (Estrada
et al., 2000, 2003; Passaquin, Lhote and Rüegg, 1998). These
findings are important because Ca2+ triggers the muscle contraction and regulates energy metabolism (Berchtold, Brinkmeier
and Muntener, 2000).
Hormones can influence other neural pathways important to
muscle function. Early research identified rapid C effects upon
the electrophysiological properties of the diaphragm muscle in
rats (Dlouhá and Vyskočil, 1979), and rapid T effects upon the
reflex activity of rat penile muscle (Sachs and Leipheimer,
1988). More recently, an increase in T concentrations was
found to be effective in decreasing the cortical motor threshold
in humans (Bonifazi et al., 2004), whereas C concentrations had
a direct effect upon the motor cortex and electromyographic
activity of hand muscle in humans (Sale, Ridding and
Nordstorm, 2008). Collectively, these rapid hormonal effects
have possible implications for muscle function. In fact, correlations have been reported between hormone concentrations and
individual performance during speed, power, and strength tests
(Bosco et al., 1996a, 1996b; Crewther et al., 2010; Jürimäe and
Jürimäe, 2001; Słowińska-Lisowska and Witkowski, 2001).
The rapid effects of T and C could also play a role in controlling
muscle growth, since the expression of performance (e.g. forces
produced, work done) during individual workouts is a major
factor influencing protein metabolism (Crewther, Cronin and
Keogh, 2005).
2.4.5 GROWTH HORMONE
RESPONSES TO RESISTANCE TRAINING
GH is another anabolic hormone which influences muscle
growth by increasing protein synthesis and reducing muscle
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protein degradation (Crewther et al., 2006; Velloso, 2008).
The release of GH may further enhance the training environment by stimulating the release of a family of polypeptides
called the somatomedins from the liver (Velloso, 2008); this
family is also known for its anabolic effects upon muscle tissue.
Unlike the steroid hormones, human GH represents a family of
proteins rather than a single hormone complex, with over 100
forms of GH currently identified within plasma fluid (Baumann,
1991). However, the function of the different variants of GH
has not yet been fully established. The most dominant form of
GH in circulation, and the most widely examined within
research, is the 22kD variant.
2.4.5.1
Effects of workout design
Similar to the steroid hormones, GH is also acutely responsive
to the design of different training workouts. Hypertrophy training sessions have, for example, been shown to produce large
increases in circulating GH concentrations, and more so than
maximal-strength training sessions (Häkkinen and Pakarinen,
1993; Kraemer et al., 1990, 1991, 1993; Smilios et al., 2003;
Zafeiridis et al., 2003). Much less research has investigated the
hormonal responses to an explosive power workout in males
and females (Linnamo et al., 2005), with GH increasing after
exercise, but only in men. It is interesting to note that the magnitude of the acute changes in GH (up to 170-fold) after different training sessions is generally much greater than that
observed for T (up to 1-fold) and C (up to 2-fold), relative to
baseline measurements (Crewther et al., 2006).
2.4.5.2
Effects of age and gender
A reduction in the GH response to resistance exercise is seen
during later life. Häkkinen and Pakarinen (1995) compared the
GH responses of three groups of males (27 years, 47 years, 68
years) and females (25 years, 48 years, 68 years), each performing an identical weight-training session. For males, the
27-year-old group reported the greatest GH response (200fold), followed by the 47-year-olds (19-fold), with no changes
reported in the 68-year-olds. For females, the 48-year-old group
produced a much larger increase in GH (20-fold) than the
25-year-olds (2-fold), while the oldest female group was nonresponsive to the exercise protocol. Other research findings are
in agreement (Häkkinen et al., 1998, 2000; Kraemer et al.,
1998a, 1999; Pyka, Wiswell and Marcus, 1992) and confirm
that the decline in muscle size and performance with age may
be partially attributed to changes in GH activity. No significant
differences in GH concentrations were found between men and
boys (Pullinen et al., 2002).
Males generally attain greater acute GH responses (relative
changes) to resistance than females (Häkkinen and Pakarinen,
1995; Häkkinen et al., 2000, 2002; Kraemer et al., 1991;
Pullinen et al., 2002). On the other hand, females have been
shown to produce greater GH responses (absolute values) after
a single training session (Häkkinen et al., 2000; Kraemer et al.,
c12.indd 158
1991, 1998b). These findings may be related to the oestrogen
senitization of the somatotrophs, which are known to give an
increased responsiveness to a variety of stimuli among females
(Kraemer et al., 1991), and/or baseline differences in GH concentrations, which are greater for females (Kraemer et al., 1991;
Pullinen et al., 2002). The importance of elevated GH among
females requires further investigation. It is noteworthy that
most studies have examined females during the follicular phase
of menstruation (Consitt, Copeland and Tremblay, 2001;
Copeland, Consitt and Tremblay, 2002; Kraemer et al., 1991,
1993, 1998b; Mulligan et al., 1996; Pullinen et al., 2002; Taylor
et al., 2000). Clearly, the effects of resistance exercise on
hormone release in different phases of the menstrual cycle is
another area warranting investigation.
2.4.5.3 Effects of training history
The GH response to a resistance training sessions does not
appear to be influenced by training history. For instance, no
differences in the acute GH responses were found between
trained and untrained athletes (Ahtiainen et al., 2004), or as a
function of weight-training experience (Kraemer et al., 1992).
Likewise, resistance training of varying periods produced little
or no change in the GH responses (Häkkinen et al., 2001;
Kraemer et al., 1998b, 1999; McCall et al., 1999; Nicklas
et al., 1995). Taylor et al. (2000) did report a greater GH
response to resistance exercise among trained females (90%)
when compared to untrained females (30%). This result may be
partially attributed to the significantly lower resting GH values
for the trained group. Disparate findings in this area may also
be attributed to individual variability in the GH responses to
exercise and different training methodologies, as well as possible interactions with age and gender.
2.4.6
OTHER BIOCHEMICAL
MARKERS
The mammalian target of rapamycin (mTOR) is one of the more
recently discovered pathways that appear important for hypertrophy (Drummond et al., 2009a; Terzis et al., 2008). Possibly
the most influencial study in this area is that of Terzis et al.
(2008); using an indirect measure of mTOR activation, via
muscle biopsy tissue, a strong relationship (r = 0.81–0.89) was
seen between the hypertrophy and strength gains achieved over
a 14-week training period and mTOR activity. Taken together
with other studies, in which rapamycin treatment can prevent
resistance exercise-induced hypertrophy (Drummond et al.,
2009b), this is good evidence of an involvement of mTOR in
muscle adaptation. However, biopsy assessments are somewhat
longitudinally limited when compared to blood or saliva analyses and comprehensive data relating mTOR to training adaptation with different protocols remains to be collected. Likewise,
very few systematic studies have investigated the modulating
effects of age, gender, and training history upon mTOR.
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Insulin is also believed to have a strong anabolic effect upon
muscle growth, repair, and recovery (Crewther et al., 2006;
Kraemer, 2000). Whilst the actions of the other anabolic hormones would appear to directly influence cellular reactions and
protein accretion, by either binding directly inside the cell
(steroid hormones) or to the cell membrane (peptide hormones),
the actions of insulin mediate the adaptive processors involved
in tissue regeneration and growth (Crewther et al., 2006;
Kraemer, 2000). The catecholamines norepinephrine and epinephrine also help to mediate weight-training adaptation, although
this role is probably related to neuromuscular function, energy
mobilization, and utilization, as well as preparing individuals
for the stress of resistance exercise (French et al., 2007; Zouhal
et al., 2008). Few data are available concerning the acute
response patterns of these hormonal markers to different resistance training workouts and long-term adaptation.
2.4.7 LIMITATIONS IN THE USE
AND INTERPRETATION OF
BIOCHEMICAL MARKERS
Biochemical markers can be regarded as simple markers; that
is, their changes mirror or predict changes in performance or as
causal agents (blocking their effect abolishes any expected
gains in performance). They can also be regarded as permissive
(as long as they are present in physiological quantities the performance changes can occur) or dose-dependent (the relationship to performance depends on the dose present). Three areas
have been investigated. In the case of T, blocking its effect on
androgen receptors prevents resistance training-induced hypertrophy and strength changes (Kvorning et al., 2006; Inoue
et al., 1994). Whether this is permissive or has a dose-response
nature is not as yet known. Clearly, supraphysiological levels
of T are associated with extreme hypertrophy, and very low
levels (hypogonadism) with loss of muscle mass and strength
(alleviated by returning T to physiological levels).
The roles of GH and IGF-1 remain more equivocal. Although
mechanical stimulation increases IGF-1, studies have shown
that functional IGF receptors are not needed for hypertrophy to
occur (Spangenburg et al., 2008), in contrast to the apparent
permissive necessity of T. Recent data suggest that IGF-1 may
be of greater importance in inducing connective tissue adaption
than in inducing muscle growth per se (Yakar et al., 2009).
Other biochemical pathways and hormones have not been
investigated to the same extent as T, C, and GH, but may have
overlapping observations with the above. It is highly likely that
an orchestra of biochemical factors are needed for resistance
training adaptation to occur.
The most obvious difficulty in trying to assess biochemical
markers relative to resistance training adaptation is the disparity
of methods and protocols across studies, as well as the use of
non-uniform training-status populations. Many studies use a
single-point assay when frequent longitudinal sampling is
needed to adequately understand the dynamics of hormonal
response to resistance exercise. Similarly, sampling methods
c12.indd 159
159
– saliva, blood (venous or capillary), tissue – differ, as do protocols. Control data is generally inadequate and often fails to
take into account such variables as time of day, given the circadian rhythm of hormones (Kraemer et al., 2001; Nindl et al.,
2001a; Thuma et al., 1995). This understanding can be further
confounded by the pulsatile secretion of some hormones (e.g.
GH) (Nindl et al., 2001b). Plasma volume changes during
resistance exercise, mainly due to an accumulation of lactate
and other metabolites in the muscles (Durand et al., 2003;
Wallace, Moffatt and Hancock, 1990), can potentially change
the measured concentrations of hormones, irrespective of actual
changes in hormone production.
Saliva is a relatively new format for the measurement of
hormones, compared to blood and muscle sampling, and offers
an easy compliant method that can be applied frequently with
relatively low stress (Cook, 2002; Vining and McGinley, 1986).
Furthermore, saliva reflects the biologically active component
of the steroid hormones, since only the free hormone partitions
cross blood into saliva (Vining and McGinley, 1986; Viru and
Viru, 2001). However, the contamination of saliva with blood
and salivary protein from the mucosa can interfere with hormonal measurements (Tremblay, Chu and Mureika, 1995). The
partitioning of hormones between blood and saliva (e.g. time
lag, influence of flow rate, etc.), particularly under stress is also
curretnly not well known. Assay selection adds another variable, with different antibodies and assays used by suppliers,
producing different cross-reactivity and potentially different
results (Tremblay, Chu and Mureika, 1995).
2.4.8 APPLICATIONS OF
RESISTANCE TRAINING
Applications of the literature to resistance training are extremely
difficult, in large part due to the lack of standardization of
design. Sampling points, assay designs, and hormonal fraction
examined all vary greatly, and in many cases subjects are naïve
resistance trainers of variable age. Consistent pattern studies are
needed in elite athletes in order to understand the usefulness, if
any, of hormones in patterning of training adaptation. It seems
likely that the endocrine response to resistance exercise plays
an important role in facilitating changes in both maximal
strength and power and, at least to some extent, through morphological adaptation. In conjunction with mechanical stimuli,
stimulation of multiple pathways including mTOR hormones
probably assists in the remodelling of muscle tissue (i.e. protein
synthesis and degradation) post-exercise. Over time, a net
increase in protein synthesis should increase muscle fibre area
and thereby lead to greater CSA of the gross muscle. Resistance
exercise is also suggested to be capable of modulating the
‘quality’ of muscle protein synthesized (Goldspink, 1992,
2003). However, it is likely that hormones also act to effectuate
other changes that contribute to power and strength.
Resistive exercise programmes used for hypertrophy generally elicit the largest anabolic (e.g. T, GH) responses, which are
theoretically conducive to the accretion of protein and muscle
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size. However, mTOR is also strongly stimulated by these types
of workout, and antagonizing either T or mTOR, as discussed
earlier, severely hampers hypertrophy. Hypertrophy workouts
also elicit the largest C responses, traditionally regarded as
catabolic. In breaking down muscle protein the catabolic actions
of C may create an increased pool of amino acids, enabling
protein synthesis to occur, or increase protein turnover rate in
previously inactive muscles (Viru and Viru, 2001), aiding the
remodelling of muscle protein. Typically, maximal-strength
workouts produce smaller hormonal responses (and mTOR has
yet to be explored outside standard hypertrophy models), suggesting that the remodelling of muscle tissue is less likely to
occur. Strength athletes (i.e. bodybuilders and power lifters/
Olympic lifters) are also characterized by different morphological profiles (Alway et al., 1992; Tesch, 1987; Tesch and
Larsson, 1982; Tesch, Colliander and Kaiser, 1986), anecdotally supporting these underlying hormonal differences.
Power-loading workouts also elicit smaller hormonal
responses, and do not produce as much apparent change in
muscle CSA, compared to hypertrophy workouts. Endurance
exercise can, under some circumstances, produce significant
increases in circulating hormone levels, similar to those changes
seen across hypertrophy workouts (Consitt, Copeland and
Tremblay, 2001; Kindermann et al., 1982; Thuma et al., 1995;
Zafeiridis et al., 2003), but these do not generally result in any
substantial changes in muscle size, which is perhaps attributable
to a lack of the necessary mechanical stress. Thus, other
mechanical factors (e.g. total tension, work done, time under
tension) associated with the training stimulus may determine
whether or not morphological adaptation will occur, and again
mTOR mechanisms are not know for these types of training
protocol.
Obviously the design of resistance training workouts plays
an important role in determining the acute hormonal response.
However, other factors such as training status, type of training
experience, gender, age, nutrition, and genetic predisposition,
all of which are highly individual, can also influence the hormonal responses. Where one pathway may become saturated or
unavailable, another may alter its contribution to make the
hormonal response a dynamic feature over time. The T/C has
proven to be a sensitive tool for monitoring individual changes
in power and/or strength during periods of training and detraining (Alén et al., 1988; Fry et al., 2000; Häkkinen et al.,
1985, 1988; Raastad et al., 2001). Recently, Haff et al. (2008)
demonstrated that the changes in the T/C could predict temporary over-reaching (or lack of recovery) in a group of elite
female weightlifters and that these T/C changes matched well
with transient deficits in force–time curves (Haff et al., 2008).
Beaven et al. (2008b) presented a different opinion on the
classical hypertrophy–power–maximal strength workouts.
When they applied these workouts to well-trained professional
c12.indd 160
rugby players, overall group data suggested little T response
to any of the protocols and a fall in C across all protocols
(Beaven, Gill and Cook, 2008a). After re-examining the data
on an individual basis, there were marked and significant differences, with some of the athletes responding with large
increases in T to hypertrophy, others to strength, and still
others to power workouts. This individual-workout-dependent
response appeared reasonably stable over a three-week period.
Beaven and co-authors went on to show that utilizing these
individual responses could produce greater hypertrophy and
strength gains than any of the other protocols (Beaven, Cook
and Gill, 2008b). There are limitations in this study, such as
the small sample size used, but it a reasonably valid conclusion
to suggest that much of the variability seen in the literature
across resistance training protocols may be due to large consistent individual differences.
Biochemical monitoring has the potential to greatly improve
our understanding of resistance training adaption and ultimately
to assist in accelerating acquisition of its features of hypertrophy, power, and strength. However, we are still a considerable
distance away from achieving this. Consistency in the study
protocols, athletes used, and type of hormonal biochemical
monitoring are needed. Limitations in the elite athlete world
will include sampling; for example, while mTOR appears fascinating at present, it requires muscle biopsy for its assessment.
Planning frequent longitudinal sampling based on biopsy is
extremely difficult in elite athlete tracking. In contrast, saliva
collection is extremely easy, but may suffer from the fact that
we are only examining the free component of the hormonal
pool, with time lags relative to other body pools that are currently poorly understood. The goals are tangible but will require
good consistency across a number of studies to be achieved.
2.4.9
CONCLUSION
The contribution of biochemical markers to hypertrophy,
strength, and power development, while tangible, are far from
fully elucidated. Similarly, the actual roles of different resistance workouts in producing different muscle outcomes are also
questionable. To provide further understanding in these areas,
research needs to adopt a more systematic approach when evaluating biochemical changes. The differences between non-elite
and elite athletes also need addressing and any approach made
should have sufficient athlete compliance to collect a rich longitudinal base of both biochemical and related performance
data. Collectively, this information would not only provide a
better understanding of the roles of different biochemical processes in mediating resistance training adaptation, but would also
lead to the effective prescription of training protocol on an
individual-athlete basis.
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CHAPTER 2.4
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2.5 Cardiovascular Adaptations to
Strength and Conditioning
Andrew M. Jones and Fred J. DiMenna, School of Sport and Health Sciences, University of Exeter, Exeter, UK
2.5.1
2.5.2.2
INTRODUCTION
During a lifetime, the cardiovascular system of an average
person will be responsible for the movement of over 200 million
litres of blood just to sustain life at rest. Add in the extra work
necessary to support all of our daily physical activities and it is
obvious that the human cardiovascular system must operate as
efficiently and effectively as any machine that man has ever
made. The purpose of cardiovascular strength and conditioning
training is to systematically overload cardiovascular function
so that specific components of the system that might limit its
capacity will improve their level of performance.
2.5.2
CARDIOVASCULAR FUNCTION
2.5.2.1
Oxygen uptake
The cardiovascular system plays a vital role in maintaining
cellular homoeostasis, especially during exercise. For example,
when exercise is initiated and muscles begin to contract vigorously, aerobic energy metabolism within active muscle cells
increases in an attempt to support the higher level of energy
turnover. This mandates a coordinated effort by the pulmonary
and cardiovascular systems to ensure that sufficient atmospheric oxygen is delivered to the mitochondria of the involved
fibres. The Fick equation indicates that the quantity of oxygen
that will be consumed (oxygen uptake; VO2) is a function
of both the amount contained in the blood that leaves the
heart and the quantity removed from that blood as it perfuses
active tissues. Oxygen consumption is proportional to the
intensity of the contractions being performed and in elite
athletes can surpass 20 times the resting requirement at
maximal levels of exertion. This means that critical cardiovascular adjustments must occur to facilitate delivery of the
appropriate amount of oxygenated blood to the body’s periphery during exercise.
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
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Maximal oxygen uptake
Maximal oxygen uptake (VO2max) represents the maximum rate
at which oxygen can be consumed by a human at sea level.
Therefore, VO2max is often considered to reflect functional
capacity and is typically used as an index to assess cardiovascular function. During exercise at sea level that requires more
than approximately one third of an individual’s total muscle
mass, it is generally accepted that VO2max is principally limited
by the rate at which oxygen can be supplied to the muscles and
not by the muscles’ ability to extract oxygen from the blood
they receive (Andersen and Saltin, 1985; Gonzalez-Alonso and
Calbet, 2003; Knight et al., 1993; Saltin and Strange, 1992;
Wagner, 2000). Total blood volume for an average adult is
approximately 5 l, and this blood can carry a maximum of
180–200 ml of oxygen per litre in a healthy individual at sea
level (Brooks et al., 2000). Given that the cardiovascular system
is a closed system (additional blood cannot be added when
circulatory demands are high), this means that prodigious
VO2max values can only be attained if the limited amount of
blood that is available for distribution is both sent to and
returned from the active musculature very rapidly.
2.5.2.3
Cardiac output
Cardiac output is the volume of blood ejected from the left
ventricle of the heart each minute. Elite endurance athletes
who can achieve VO2max values of over 5–6 l/min must generate cardiac outputs well in excess of 30 l/min to do so (Jones
and Poole, 2009). Cardiac output can be calculated as the
product of heart rate (myocardial contractions per minute) and
stroke volume (millilitres of blood ejected per contraction),
and both of these variables increase during exercise (see Figure
2.5.1). Maximum heart rate is relatively fixed for a given
individual at a given point in time, although it does decrease
with age. Conversely, maximum stroke volume is a trainable
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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PARASYMPATHETIC
WITHDRAWAL
PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
SYMPATHETIC
ACTIVATION
O2
CO2
FRANK STARLING
≠ MYOCARDIAL
CONTRACTILITY
≠ HEART
RATE
≠ PULMONARY
BLOOD FLOW Æ
≠ CARDIAC PRELOAD
≠ STROKE
VOLUME
≠ VENOUS RETURN Æ
≠ PULMONARY
BLOOD FLOW
≠ CARDIAC OUTPUT
VASODILATION OF ACTIVE MUSCLE
VASCULAR BEDS Æ
≠ MUSCLE BLOOD FLOW
MUSCLE PUMP +
MAINTAINED CENTRAL PRESSURE Æ
≠ VENOUS RETURN
SYMPATHETIC
ACTIVATION
≠ MUSCLE BLOOD FLOW +
≠ MUSCLE O2 EXTRACTION Æ
≠ O2 CONSUMPTION
≠ O2 CONSUMPTION
Æ
≠ CO2 PRODUCTION
VASOCONSTRICTION OF
VISCERAL, RENAL AND INACTIVEMUSCLE VASCULAR BEDS Æ
MAINTENANCE OF CENTRAL
BLOOD PRESSURE
Figure 2.5.1 Endurance exercise provides the precise stimulus that is specific for inducing positive cardiovascular adaptations. When large
muscle groups contract rhythmically at a sustainable percentage of the maximal voluntary contraction, aerobic metabolism predominates and the
deliverance of atmospheric oxygen to the body’s periphery must increase. Consequently, circulation is elevated and the pumping action of the
muscles ensures that blood returning to the heart is similarly enhanced. This results in eccentric left-ventricular hypertrophy because the heart’s
chambers must expand from the inside out in order to accommodate more blood. Illustration by Jamie Blackwell
physiological parameter that is determined by the ability of
the left ventricle to accommodate blood during diastole (the
relaxation phase of the cardiac cycle) and to eject the blood
it contains during systole (the cardiac contraction). For many
years, exercise physiologists believed that stroke volume
reached a plateau at approximately 40% of VO2max, after which
heart rate was the sole mechanism for increasing cardiac output
(Åstrand et al., 1964). However, more current research indicates that this is not the case, at least for highly-trained endurance athletes, because in these individuals stroke volume
continues to rise throughout incremental exercise to exhaustion
(Glehdill, Cox and Jamnik, 1994; Wiebe et al., 1999; Zhou
et al., 2001). Regardless of this distinction, however, maximal
heart rate and maximal stroke volume together determine
maximal cardiac output, which has been estimated to account
for 70–85% of the limitation to VO2max (Bassett and Howley,
c13.indd 166
2000), and it is stroke volume that can be predominantly altered
by training.
2.5.2.4 Cardiovascular overload
With regard to exercise training, the principle of specificity
states that the structural and functional adaptations that can be
expected to result from repeated application of a given overload
exercise stressor will be unique and highly dependent on the
particular stressor. Therefore, identifying the appropriate training stimulus requires knowledge of the system being targeted
in order to determine the specific form of exercise that will
maximally tax its principal function. Given that the cardiovascular system’s primary purpose is to circulate blood, the only
forms of exercise that will be optimal for inducing positive
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CHAPTER 2.5
CARDIOVASCULAR ADAPTATIONS TO STRENGTH AND CONDITIONING
adaptations in cardiovascular function are those that require
rapid movement of blood to and from the body’s periphery.
Unfortunately, there is often a lack of understanding in the
strength and conditioning field regarding the precise overload
that achieves this purpose.
2.5.2.5 The cardiovascular
training stimulus
It has long been known that VO2 and heart rate rise in an
approximately linear manner as exercise intensity is increased
(Åstrand and Saltin, 1961). This has led to the use of heart rate
as a convenient gauge of VO2 and therefore cardiovascular
training intensity (Burke, 1998). However, it is important to
recognize that an elevated heart rate per se is not the requisite
stimulus that drives chronic cardiovascular adaptations. For
example, during conventional resistance training (i.e. muscular
contractions performed against a relatively high percentage of
the maximal voluntary contraction), heart rate and VO2 will be
dissociated because elevation of the former will occur due to a
drive for motor unit recruitment that is mediated by the sympathetic branch of the autonomic nervous system. Furthermore,
the intense contractile effort that characterizes each repetition
and the corresponding increase in intramuscular pressure will
trap blood in peripheral vascular beds, thereby reducing blood
flow until the ‘sticking point’ of each repetition is surpassed
(Shepherd, 1987). This is not consistent with the specific overload that drives positive cardiovascular adaptation.
2.5.2.6
Endurance exercise training
Endurance exercise training is a broad term that is used quite
liberally in the field of strength and conditioning. Generally
speaking, endurance exercise has been suggested to include all
of those (usually continuous) sports events or physical activities
that rely predominantly on oxidative metabolism for energy
supply, provided that they are sustained for a sufficiently long
period of time (e.g. ≥90 seconds during high-intensity exercise
and ≥10 minutes during submaximal exercise) (Jones and
Poole, 2009). Endurance (aerobic) exercise is characterized by
rhythmic contractions of a significant portion of the body’s
larger muscle groups at a sustainable percentage of the maximal
voluntary contraction; this type of effort will also elevate heart
rate. However, in this case, VO2 is similarly increased, circulation is promoted, and an overload specific to circulatory function can be achieved (see Figure 2.5.1). This represents the
precise stimulus that induces cardiovascular adaptations, which
will be reflected in an increased functional capacity. Generally
speaking, intense endurance training results in a VO2max increase
of approximately 20%; however, greater increases are possible
if a participant’s initial fitness level is low (Brooks et al., 2000;
Hickson et al., 1981). The duration of the training programme
and the intensity, duration, and frequency of individual training
sessions are critical factors which determine the magnitude of
the increase that can be expected (Wenger and Bell, 1986). The
c13.indd 167
167
genetic proclivity for improvement and the age of the participant also play important roles.
2.5.3 CARDIOVASCULAR
ADAPTATIONS TO TRAINING
Endurance exercise training facilitates numerous chronic positive changes that affect both central and peripheral aspects of
cardiovascular system function. In addition, the heart itself
operates much more efficiently in the trained state, with a
reduced heart rate and requirement for oxygen at rest and during
submaximal exercise at the same metabolic rate (Barnard et al.,
1977). These adaptations are responsible for marked changes in
aerobic fitness, which typically manifest as an increased VO2max
and the ability to perform all submaximal exercise challenges
with reduced cardiovascular stress (see Figures 2.5.2 and 2.5.3).
2.5.3.1 Myocardial adaptations to
endurance training
Increased stroke volume/cardiac output
The most significant positive cardiovascular adaptation to
chronic endurance training is a marked increase in stroke
volume at rest and during submaximal and maximal exercise
(Ekblom and Hermansen, 1968; Saltin et al., 1968). In the
trained state, cardiac output at rest and at any absolute submaximal work rate is either unchanged or decreased (Brooks et al.,
2000). This means that the increased capacity to move blood
with each contraction of the myocardium allows any submaximal cardiac output, including the requirement at rest, to be
established at a lower heart rate (see Figure 2.5.2). Furthermore,
the maximal heart rate is also unchanged or slightly decreased
after training (Ekblom et al., 1968; Wilmore et al., 2001), but
maximal cardiac output is increased by 30% or more (Saltin
and Rowell, 1980). This means that increased stroke volume
provides the exclusive means by which maximal cardiac output
is increased due to training (see Figure 2.5.3). This improvement also represents the predominant mechanism that facilitates
an increased VO2max because only a modest enhancement of
arteriovenous oxygen difference (which reflects the ability to
extract oxygen from the blood as it circulates through active
tissues) at maximal exercise is typically present in the trained
state (e.g. 16.5 compared to 16.2 ml of oxygen per 100 ml of
blood) (Brooks et al., 2000). Training-induced increases in
stroke volume are achieved when the ventricle is able to accommodate more blood and/or when it can eject a greater percentage of the blood that it contains.
Increased left-ventricular
end-diastolic volume
The increase in maximal stroke volume that occurs due to
endurance training is predominantly attributable to an increased
quantity of blood available for ejection (Brandao et al., 1993;
Ehsani, Hagberg and Hickson, 1978; Levy et al., 1993). During
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ECCENTRIC LEFT VENTRICULAR
HYPERTROPHY
≠ TOTAL BLOOD VOLUME
≠ LEFT VENTRICULAR
END-DIASTOLIC VOLUME
≠ FRANK STARLING
≠ STROKE VOLUME
´ CARDIAC OUTPUT
≠ EJECTION
FRACTION
Ø HEART RATE
´ VO2
Ø RATE PRESSURE
PRODUCT
Figure 2.5.2 Endurance exercise training results in eccentric left-ventricular hypertrophy and an increase in total blood volume. This allows the
same submaximal exercise work rate/VO2 to be maintained at a lower heart rate and RPP
ECCENTRIC LEFT VENTRICULAR
HYPERTROPHY
≠ TOTAL BLOOD VOLUME
≠ LEFT VENTRICULAR
END-DIASTOLIC VOLUME
≠ STROKE VOLUME MAX
≠ CARDIAC OUTPUT MAX
≠ ACTIVE MUSCLE
BLOOD FLOW MAX WITH
CENTRAL PRESSURE
MAINTAINED
´ HEART RATE MAX
≠ VO2 MAX
Figure 2.5.3 Endurance exercise training results in eccentric left-ventricular hypertrophy and an increase in total blood volume. This loosens
the central circulatory restriction at maximal exercise, which allows a greater VO2max to be achieved
diastole, the ventricles relax and the blood that will be expelled
during the ensuing contraction phase fills the emptied chambers. Left-ventricular end-diastolic volume (LVEDV) or
preload is the amount of blood contained in the left ventricle
once this filling phase is complete. The amount of oxygenated
blood available for filling is dependent upon the amount of
deoxygenated blood that was sent to the lungs from the right
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ventricle of the heart during the preceding myocardial contraction. Consequently, the critical determinant of preload is venous
return (the flow of deoxygenated blood back to the right side
of the heart from the periphery). An endurance exercise session
provides a prolonged period during which venous return is
greatly increased due to the rhythmic contractions performed
by the active musculature (the muscle pump) (see Figure 2.5.1).
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Regular endurance exercise therefore mandates an adaptive
change in ventricular volume to accommodate this oftencountered overload.
Left-ventricular eccentric hypertrophy
Investigations that have used echocardiography or magnetic
resonance imaging (MRI) to measure myocardial dimensions
have revealed that athletes involved in endurance-training
sports possess increased left-ventricular mass (Cohen and
Segal, 1985; Henriksen et al., 1996; Maron, 1986; Milliken et
al., 1988; Riley-Hagan et al., 1992; Scharhag et al., 2002). This
indicates that when the heart is subjected to extended periods
of elevated venous return on a regular basis, the chronic volume
overload causes myocardial tissue to adapt. Specifically, the
muscle cells (cardiocytes) which make up the myocardium
grow larger and the myocardium as a whole grows bigger from
the inside out (Morganroth et al., 1975). This eccentric hypertrophy results in larger chambers that can accommodate more
blood. Left-ventricular eccentric hypertrophy is the critical
adaptation that allows for increased preload and it’s important
to note that this myocardial growth occurs exclusively in a
longitudinal direction, without a corresponding change in the
length of the muscle’s contractile units (sarcomeres) (Moore,
2006). Consequently, the training-induced increase in preload
that can be achieved due to left-ventricular eccentric hypertrophy causes myocardial sarcomeres to experience greater stretch
during diastole. A training-induced increase in left-ventricular
end-diastolic diameter can be achieved from as little as 10
consecutive days of cycle ergometer training (Mier et al., 1997).
The Frank–Starling mechanism
The length–tension relationship of skeletal muscle indicates
that there is a specific sarcomere length at which the contractile
myofilaments (actin and myosin) are aligned to provide the
greatest opportunity for cross-bridge interaction. This is the
optimal length for tension development in a passive setting.
However, a muscle fibre also contains series elastic components
that absorb energy when the fibre is placed on stretch.
Consequently, during active tension development, a contraction
can benefit from this ‘potential energy of elongation’ through
the stretch–shortening cycle (SSC). The Frank–Starling mechanism involves similar storage and subsequent use of elastic
energy by the muscle fibres of the heart. Frank–Starling facilitation allows for strong myocardial contractions during endurancetraining sessions when venous return and cardiac preload are
high (i.e. when left ventricular myocardial tissue is placed on
significant stretch) (see Figure 2.5.1) and the resultant eccentric
left-ventricular hypertrophy, without a corresponding increase
in myocardial sarcomere length, ensures that these stretch–
shortening properties are enhanced in the trained state (Levine
et al., 1991).
Increased myocardial contractility
An endurance-trained heart consists of compliant tissue that can
relax sufficiently to allow optimal filling of the enlarged left
ventricle during diastole. However, an increased ability to
accommodate blood will only prove beneficial if a significant
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169
portion of that blood can be expelled. The ejection fraction is
the percentage of end-diastolic volume that is pumped from the
ventricles each time the myocardium contracts. Enhancement
of the Frank–Starling mechanism due to a training-induced
increase in preload is one way that the trained heart achieves
adequate emptying. However, there is evidence to suggest that
architectural changes that facilitate a more forceful myocardial
contraction also occur due to endurance training.
In addition to intrinsic growth of the heart’s chambers, myocardial tissue can also become enlarged (hypertrophied) due to
increased synthesis of actin and myosin. A greater presence of
these contractile proteins will allow for a more forceful contraction; a heart that has thickened in this way due to exercise
training is referred to as an ‘athlete’s heart’. However, this
generic description is complicated by the fact that different
athletes overload their hearts in different ways. For example,
sports like weight lifting and wrestling involve transient periods
of work against heavy resistance to blood flow (afterload),
which is unlike the overload present during endurance exercise.
Originally, this led to a distinction of two forms of athlete’s
heart: a strength-trained myocardium, characterized exclusively
by increased wall thickness (concentric ventricular hypertrophy) and an endurance-trained heart with minimal wall growth
relative to the increased chamber size (Mitchell et al., 2005;
Morganroth et al., 1975). It is now believed that there is more
cross-over between these two effects (Pluim et al., 2000) and a
considerable increase in wall thickness can also occur in
endurance-trained athletes (Spirito et al., 1994). However, any
thickening of myocardial tissue due to endurance training is
approximately proportional to the increase in chamber dimension that occurs concurrently. Furthermore, while a 12% disproportionate increase of wall thickness compared to chamber
volume has been reported for strength-trained athletes (Fagard,
1997), the extent of this concentric ventricular hypertrophy is
relatively modest compared to the pathological changes that
occur when hypertrophic cardiomyopathies are present
(Pelliccia and Maron, 1997).
Much like skeletal muscle, an increase of contractile proteins within the myocardium allows for a stronger muscular
contraction. There is also evidence to suggest that the specific
type of myocardial contractile protein is altered with training,
as a myosin isoform that is more energetically active (myosin
V1) has been reported in the myocardial tissue of swim-trained
rats (Pagani and Solaro, 1983). However, swim training can
also enhance stroke volume and cardiac output in rats without
this conversion so this is not an obligatory feature of a trained
heart (Sharma, Tomanek and Bhalla, 1985). Trained rats also
demonstrate greater calcium storage capacity in myocardial
sarcoplasmic reticulum and increased sarcolemmal calcium flux
(Penpargkul et al., 1977; Tibbits et al., 1981). These traininginduced improvements in the ability to regulate calcium availability may improve cardiac performance, especially when
pathological compromise is present (Moore, 2006).
Training-induced bradycardia
Bradycardia is defined as a heart rate that is abnormally low;
for example, below 60 beats per minute at rest. In patient
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populations, bradycardia can be caused by chronotropic impairment due to diseases that compromise electrical conductivity
within the myocardium. However, at the other end of the spectrum, a trained heart will also beat less frequently at rest and
during submaximal exercise at the same absolute and relative
exercise intensity because it can accommodate and eject more
blood with each contraction (Blomqvist and Saltin, 1983;
Wilmore et al., 2001). Consequently, training-induced bradycardia is actually a beneficial cardiac dysrhythmia.
Myocardial work and the associated oxygen requirement of
the heart during any physical activity can be determined from
the rate–pressure product (RPP; the product of systolic blood
pressure and heart rate). For example, symptoms of limited
blood flow (i.e. insufficient oxygen supply) through coronary
arteries (e.g. angina pectoris) typically manifest at a reproducible RPP (oxygen demand) (Clausen and Trap-Jensen, 1976).
Training-induced bradycardia is therefore a beneficial cardiovascular adaptation because it allows the resting systemic circulatory requirements and those associated with any submaximal
level of physical exertion to be met with less work on the part
of the myocardium (i.e. at a lower RPP; see Figure 2.5.2).
A relatively low heart rate also provides a longer period of
diastole before an ensuing cardiac contraction, which is necessary because more time is needed to completely fill the more
compliant trained chambers (Brooks et al., 2000). Consequently,
training-induced bradycardia is an important adaptation as it
contributes to the increased stroke volume that is present at rest
and during submaximal exercise in the trained state. It is also
interesting to note that in addition to resting and submaximal
work, a number of investigations have reported that maximal
heart rate is reduced after training (on average, six beats per
minute; see Zavorsky, 2000 for review). There are numerous
training-induced adaptations that might be responsible;
however, regardless of the mechanistic basis, this effect indicates the importance of adequate ventricular filling time for the
conditioned heart and further supports the critical role that
stroke volume plays in establishing enhanced maximal cardiac
output after training. Furthermore, an unchanged or reduced
heart rate at maximal exercise in conjunction with systolic
blood pressure that is unchanged or only slightly increased
(Wilmore et al., 2001) collectively ensures that the increase in
maximal capacity in the trained state is achieved at an RPP
(and, therefore, amount of myocardial work) that is no greater
than that which was present prior to training (Secher, 2009).
2.5.3.2 Circulatory adaptations to
endurance training
Blood redistribution during exercise
One of the biggest challenges that the cardiovascular system
faces during endurance exercise is distributing its cardiac output
to critical areas of need. At rest, the splanchnic organs (stomach,
spleen, pancreas, intestines, and liver) receive more blood flow
than any other region, while the skeletal muscles receive a
modest provision because their metabolic demands are relatively low (Rowell, 1973). However, during exercise, peak
c13.indd 170
blood flow in the active muscle mass can increase 100-fold
above the resting value (Andersen and Saltin, 1985). This
presents a problem because the cardiovascular system has a
limited amount of blood available for distribution and also has
the ability to accommodate much more than it actually contains.
Simply opening up all of its vessels to allow more blood to flow
to the active musculature without a corresponding sparing of
blood from other areas would result in a catastrophic fall in
central pressure/venous return if multiple muscles were activated. This means that blood distribution during exercise mandates precise circulatory adjustments that involve both
active-muscle vasodilation (an increase in blood-vessel radius
that reduces vascular resistance to blood flow) and visceral,
renal, and inactive muscle vasoconstriction (a decrease in
blood-vessel radius that presents an impediment to flow)
(Clifford, 2007; Rowell, 1973; Shepherd, 1987).
During challenging exercise, the sympathetic branch of the
autonomic nervous system plays a vital role in activating cardiovascular function to meet the increased demand for circulation. This influence is mediated through sympathetic nerve
fibres and also via catecholamines (epinephrine and norepinephrine) released from the adrenal glands. Sympathetic activation causes an increase in both heart rate and myocardial
contractility so that cardiac output is elevated to the appropriate
level. Sympathetic activation also protects central pressure/
venous return by promoting systemic vasoconstriction. For
example, during exercise at or near VO2max, splanchnic blood
flow is reduced by almost 80% (Rowell, 1973). However, this
drive to reduce flow to all areas of the body except the heart
and brain is opposed by countering mechanisms in active
muscles which allow for a ‘functional sympatholysis’ that
results in local vasodilation and increased perfusion (hyperaemia) (Remensnyder, Mitchell and Sarnoff, 1962; Thomas,
Hansen and Victor, 1994; Thomas and Segal, 2004). The collective effect is the ability to divert limited cardiac output from
less active tissues to the areas of greatest need.
Despite the coordinated efforts of neural and hormonal
mechanisms, peripheral feedback afferents, and metaboliterelated circulating substances, the human body still cannot
adequately redistribute blood to simultaneously protect central
pressure and support peripheral requirements during challenging endurance exercise involving large/multiple muscle groups.
In fact, there is evidence to suggest that some vasoconstriction
in active muscles also occurs during intense exercise as a consequence of activating a greater quantity of muscle than the
available cardiac output can fully support. For example, active
muscle blood flow and oxygen uptake are less during twocompared to one-legged cycling and when the arms and legs
are exercised together (Klausen et al., 1982; Secher, 2009;
Secher and Volianitis, 2006; Secher et al., 1977). Furthermore,
leg cycling after ß1-adrenergic blockade that reduces cardiac
output is characterized by active muscle vasoconstriction
(Pawelczyk et al., 1992). These examples indicate that the
quantity of blood available for distribution presents a critical
limitation to aerobic exercise performance, so it is not surprising that other chronic cardiovascular adaptations to regular
endurance exercise address this restriction.
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Increased total blood volume
It is perhaps intuitive that architectural changes that allow for
greater stroke volume per cardiac contraction will be accompanied by adaptations that increase the blood that is available for
distribution. For example, a training-induced increase in blood
volume within the cardiovascular network is responsible for
greater ventricular filling pressure during diastole, which
ensures that a larger, more compliant trained left ventricle is
optimally filled when circulatory requirements are low. This
allows a given cardiac output to be established with a greater
stroke volume and reduced heart rate at rest and during submaximal exercise (see Figure 2.5.2). Furthermore, more blood
in the system provides an increased quantity for distribution to
active muscles during intense efforts. This loosens the restriction of circulation that limits VO2max (see Figure 2.5.3).
Therefore, adaptations that provide for an increased amount of
blood in the circulatory system (hypervolemia) are critical
because they facilitate both increased cardiovascular efficiency
at rest/during submaximal exercise and the ability to surpass
previous limitations when maximal levels of work are encountered. Highly-trained endurance athletes typically possess a
20–25% larger blood volume than sedentary subjects due to a
number of training-related adaptations (Convertino, 1991). The
primary one is expansion of plasma volume (Convertino, 1991;
Kanstrup, Marving and Hoilund-Carlsen, 1992; Oscai, Williams
and Hertig, 1968).
Plasma-volume expansion
The increase in stroke volume that occurs due to endurance
training is approximately mirrored by an increase in plasma
volume (Green, Jones and Painter, 1990). This is not surprising
given the dramatic effect that plasma-volume expansion has on
left-ventricular function. For example, a 9% increase in blood
volume achieved via plasma infusion has been shown to facilitate a 10–14% increase in submaximal exercise stroke volume,
which is largely attributable to increased LVEDV (Kanstrup,
Marving and Hoilund-Carlsen, 1992). In addition to providing
more blood for expulsion, this change also exacerbates the
Frank–Starling effect (Goodman, Liu and Green, 2005).
Furthermore, central venous pressure is significantly elevated
during exercise after acute plasma-volume expansion and the
fall that normally occurs with increasing workload is eliminated
(Kanstrup, Marving and Hoilund-Carlsen, 1992). The functional significance of these hemodynamic alterations is reflected
by the 6% increase in VO2peak and 16% increase in time to
exhaustion that has been reported for exhaustive constant-load
cycle exercise after a 14% expansion of plasma volume via
clinical plasma-expanding solution (Berger et al., 2006).
There is evidence to suggest that a 10% expansion of plasma
volume can occur within 24 hours of the first endurance exercise session (Gillen et al., 1991), and an overall increase of 12%
after eight days of training has been shown (Convertino et al.,
1980, 1983). Importantly, this training-induced hypervolemia
is accompanied by a similar increase in VO2max, and a 0.78
correlation between total blood volume and VO2max expressed
relative to body weight has been reported (Convertino,
1991; Convertino, Keil and Greenleaf, 1983; Goodman, Liu and
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171
Green, 2005). This confirms the importance of blood volume
as a determinant of functional capacity. Another major benefit
of a rapidly occurring plasma expansion is that it protects
against acute fluid loss from the vascular space that occurs
during extended endurance exercise sessions; specifically,
although a similar exercise-induced plasma-volume shift occurs
in the trained state, training-induced hypervolemia ensures that
more blood remains for circulation once this shift has taken
place (Convertino, 1983). Rapidly-occurring plasma-volume
expansion is therefore an important adaptation that acclimatizes
an athlete’s cardiovascular system to prolonged heavy exercise
in the heat (Green, Jones and Painter, 1990).
The mechanism that facilitates plasma-volume expansion
after as little as one endurance exercise session appears to be
related to the plasma protein albumin, which exerts an osmotic
pull that draws fluid from the extracellular space (Gillen et al.,
1991). Plasma albumin content is elevated within one hour following a bout of intense upright cycle exercise (Nagashima
et al., 1999). Furthermore, after eight days of training, a ninefold elevation of plasma renin activity and vasopressin concentration during exercise promotes fluid and sodium retention,
which also plays a role (Convertino et al., 1980).
Increased red blood cells
For up to the initial 10 days of training, changes in plasma
volume are primarily responsible for changes in blood volume,
with little or no associated elevation of red blood cell mass
(Convertino, 1991; Convertino et al., 1980). However, the total
increase in blood volume that eventually occurs due to training
appears to be the result of both plasma-volume expansion and
increased red blood cell number (Hoffman, 2002). A greater
number of red blood cells increases the oxygen-carrying capacity of the blood; however, the increase in plasma volume outstrips the increased production of red blood cells so that
haematocrit (the relative portion of the blood comprising red
blood cells) is actually reduced in the trained state (Mier et al.,
1997). This is important because it results in decreased blood
viscosity and facilitated flow.
Improved muscle blood-flow capacity
Together, the training-induced improvement in myocardial
capacity and increased total blood volume would be of limited
use if endurance training did not also improve the cardiovascular system’s ability to perfuse the exercising musculature with
blood. Once it leaves the left ventricle through the aorta, oxygenated blood travels through large arteries to small arteries and
arterioles before accessing the interstitial space via capillaries.
Training-induced remodelling of these structures must therefore
occur on multiple levels as existing arterial vessels must be
enlarged and new capillaries must be formed. These adaptations
take place due to processes known as arteriogenesis and angiogenesis, respectively (Andersen and Henriksson, 1977; Lehoux,
Tronc and Tedgui, 2002; Prior, Yang and Terjung, 2004).
Furthermore, there is evidence to suggest that functional alterations in the vasomotor reactivity of arteries/arterioles also characterize the trained state. The degree to which these structural
and functional adaptations contribute to the improved capacity
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for muscle blood flow after training is likely the result of muscle
fibre-type composition, motor unit recruitment pattern, and the
mode/duration/intensity of the exercise that was performed (e.g.
interval sprint versus endurance training) as non-uniform adaptations between muscles of different fibre-type composition and
within the same vascular network have been reported (Laughlin
and Roseguini, 2008).
Arteriogenesis and angiogenesis
Arteriogenesis allows for greater bulk blood flow to the
periphery, while angiogenesis provides a denser capillary
network that increases red blood cell mean transit time and
decreases diffusion distance. Increased transit time through
active muscle might contribute to the higher oxygen extraction
fraction that has been observed during submaximal exercise
in the trained state (Kalliokoski et al., 2001). It is interesting
to note that strikingly different spatial patterns of adaptation
can exist in arteries compared to capillaries within and between
trained muscle, which suggests that the factors/signals promoting arteriogenesis and angiogenesis might be different
(Laughlin and Roseguini, 2008). There is also evidence to
suggest that the coronary arteries that supply blood to myocardial tissue are altered by endurance training; specifically,
an increase in diameter (Currens and White, 1961; Wyatt and
Mitchell, 1978) and an enhanced ability to dilate during exercise (Kozàkovà et al., 2000) have been reported. Furthermore,
the cardiac capillary network is enhanced and some cardiac
capillaries are transformed into arterioles due to training
(Brown, 2003).
Improved blood distribution
The trained state is characterized by reduced sympathetic
nervous system activity at any specific absolute level of submaximal exertion because the relative stress associated with the
effort is decreased (Peronnet et al., 1981). Consequently, the
reduction of blood flow to the splanchnic and renal regions
during exercise is attenuated in the trained state. This has the
potential to be beneficial because homoeostatic disturbances
associated with decreased flow are reduced and the ability to
metabolize glucose during prolonged exercise is enhanced
(McAllister, 1998). There is also evidence to suggest that there
is an altered control of vascular resistance in exercising muscle
in the trained state. For example, in some circumstances, trained
animal muscle exhibits increased endothelial-dependent dilation due to changes in endothelial nitric oxide synthase (Jasperse
and Laughlin, 2006). This enzyme generates nitric oxide, which
is an important vasodilator in the arterial network. However, it
appears as if the presence/extent of any effect of training on
endothelium-dependent dilation in the arterial network depends
on numerous factors, including the duration of the training
programme, the size and anatomical location of the artery/
arteriole, and the health of the individual (e.g. greater adaptations typically occur in diseased than in healthy individuals)
(Jasperse and Laughlin, 2006). It is also interesting to note that
endurance training and interval sprint training induce nonuniform changes in smooth muscle and endothelium throughout
c13.indd 172
the arteriolar network, which suggests a highly specific nature
to these alterations in vasomotor control (Laughlin and
Roseguini, 2008). Finally, heterogeneity of blood flow within
active muscles is also reduced in the trained state (Kalliokoski
et al., 2001). This vascular adaptation may facilitate oxygen
extraction by ensuring that blood perfusing a contracting muscle
is more uniformly distributed to specific areas of need (Piiper,
2000).
Reduced blood pressure
Regular endurance training elicits only modest reductions in
systolic and diastolic blood pressure at rest (e.g. <3 mm Hg).
However, during submaximal exercise at the same absolute
work rate, greater reductions are present (Wilmore et al., 2001).
Arterial blood pressure is a function of blood flow in the cardiovascular system (cardiac output) and resistance to flow
created by the peripheral vasculature (total peripheral resistance). Arteriogenesis/angiogenesis and reduced sympathetic
nervous system activity at rest and in response to submaximal
work are two training-induced alterations responsible for reducing total peripheral resistance and, by extension, blood pressure
in the trained state (Fagard, 2006). At maximal exercise, total
peripheral resistance is also reduced after training; however,
cardiac output is increased. The collective effect is an unchanged
or only modestly increased systolic, but decreased diastolic,
blood pressure during maximal exercise after training (Wilmore
et al., 2001).
2.5.4 CARDIOVASCULAR-RELATED
ADAPTATIONS TO TRAINING
Generally speaking, cardiovascular adaptations are directly
responsible for the enhanced functional capacity that is achieved
in the trained state. However, a training-induced increase in
VO2max is only possible if the ability to transfer oxygen to the
blood is sufficient. Similarly, an increased capacity for circulation is of no benefit if oxygen cannot be extracted from the
blood and utilized where it is required. Consequently, a
summary of cardiovascular adaptations to strength and conditioning must include mention of both the pulmonary and the
skeletal muscular systems.
2.5.4.1 The pulmonary system
Pulmonary diffusion capacity
In humans, the lungs provide the critical link that is necessary
for transport of metabolic gases to and from the atmosphere
by the cardiovascular system. Therefore, cardiovascular function is intimately related to pulmonary diffusion capacity.
However, most evidence suggests that endurance training has
little or no effect on the structure and function of the lungs
and airways (Brown, 2000; Dempsey, Miller and Romer,
2006a; Wagner, 2005). For example, lung diffusion capacity
and pulmonary capillary blood volume are not substantially
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CARDIOVASCULAR ADAPTATIONS TO STRENGTH AND CONDITIONING
different between endurance-trained and healthy untrained subjects at rest or during exercise, and static lung volumes and
maximum flow-volume loops are also similar (Dempsey, Miller
and Romer, 2006a). This has been interpreted as evidence that
pulmonary diffusion capacity exceeds cardiovascular capacity
by a sufficient margin that training-induced alterations in cardiovascular function can occur without associated pulmonary
change. One reason for this discrepancy appears to be the
degree to which each system can elevate its level of function
when challenged. During maximal exercise, 4–6-fold increases
in respiratory rate and 5–7-fold increases in tidal volume are
typically observed (Brown, 2000). Consequently, minute ventilation (the product of the two) can increase by as much as
40-fold during all-out exercise. This far outstrips the 4–5-fold
increase in cardiac output that is attainable under the same
circumstances.
Ventilatory efficiency
The robust ability to increase minute ventilation during exercise
means that training-induced cardiovascular adaptations that
allow for an increased VO2max need not be accompanied by
adaptive changes in either respiratory rate or tidal volume.
However, the trained state is characterized by a more efficient
ventilatory exchange. At the same submaximal steady-state
work rate, minute ventilation is less after training and the ventilatory equivalent for oxygen (VE/VO2 ratio) is reduced (Davis
et al., 1979). Furthermore, a given minute ventilation is achieved
with greater tidal volume and reduced breathing frequency.
This decreases the oxygen cost of ventilation and reduces ventilatory muscle fatigue, which can adversely affect performance
(Dempsey et al., 2006b).
Exercise-induced arterial hypoxaemia
Generally speaking, the alveolar partial pressure of oxygen
rises during exercise and the partial pressure of oxygen in
arterial blood is therefore maintained. However, an appreciable fall in arterial oxygen saturation (e.g. exercise-induced
arterial hypoxaemia, EIAH) is often observed during nearmaximal or maximal exercise in highly-trained individuals
possessing high VO2max values (Dempsey, Hanson and
Henderson, 1984). Furthermore, inspiration of a hyperoxic
gas mixture by subjects who experience EIAH improves both
VO2peak and performance (Wagner, 2005; Wilkerson, Berger
and Jones, 2006). The cause of this pulmonary limitation has
yet to be identified, but might relate to the prodigious maximal
cardiac outputs that these athletes can generate. For example,
the lung has a finite and relatively small capillary volume,
so an extremely high cardiac output could result in an excessively short red blood cell transit time that restricts oxygen
loading. Regardless of the mechanism, however, the presence
of a ventilatory-related restriction to maximal exercise in some
highly-trained individuals does raise the question as to why
pulmonary diffusion capacity does not improve in healthy
individuals as a consequence of endurance exercise training
(Wagner, 2005).
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173
2.5.4.2 The skeletal muscular system
Increased mitochondrial
enzyme activity
A circulatory constraint of VO2max does not mean that endurance
exercise adaptations are limited to those that facilitate enhanced
oxygen delivery. On the contrary, it is well documented that the
specific sites where oxygen is consumed (skeletal muscle mitochondria) are also dramatically altered by training. Specifically,
enzymatic activity is increased 200–300% in some mitochondrial enzymes and 30–60% in others (Holloszy and Coyle,
1984). While increases are not present in all mitochondrial
enzymes, it is interesting to note that improvements of this
magnitude far outstrip the increase in VO2max that occurs due to
training. This indicates that it is beneficial to improve mitochondrial capacity for reasons other than simply increasing the
maximal oxidative capacity of the organism.
Increased mitochondrial volume/density
A four-week programme of daily sprint training can facilitate a
VO2max increase of similar magnitude to that elicited by endurance training. However, only the latter stimulates a synthesis of
mitochondrial protein that results in greater mitochondrial
content in the trained musculature (Davies, Packer and Brooks,
1981, 1982). This proliferation is directly responsible for the
aforementioned training-induced increase in enzymatic activity
because the specific activity of mitochondrial enzymes (i.e.
enzymatic activity per unit of mitochondrial protein) remains
unaltered in the trained state (Tonkonogi and Sahlin, 2002). It
is also interesting to note that significant increases in mitochondrial content are present in all three principal fibre types
(Howald et al., 1985). Increased mitochondrial mass ensures
that any submaximal VO2 can be sustained with less metabolic
stress per mitochondrial unit.
Improved respiratory control
When mitochondrial mass is increased after training, better
respiratory control (the ability to sustain a given rate of oxidative flux with less free ADP concentration, that is at a higher
ATP : ADP ratio) is achieved and feedback activation of glycolysis at the same absolute submaximal work rate is reduced
(Bassett and Howley, 2000). Consequently, a shift in substrate
utilization will occur that is supported by the increased presence
of enzymes that mobilize and metabolize fat (Holloszy and
Coyle, 1984). The end result is that fat catabolism is increased,
glycogen is spared, and less lactate is formed during submaximal exercise in the trained state (Azevedo et al., 1998; Coggan
et al., 1993). This means that challenging exercise can be sustained for longer periods with less fatigue (i.e. endurance capacity is improved). Furthermore, in accordance with the model of
respiratory control proposed by Meyer in 1988, increased mitochondrial mass and tighter respiratory control should allow for
a more rapid VO2 response when a transition is made from a
lower to a higher metabolic rate (i.e. faster VO2 kinetics)
(Meyer, 1988). This is beneficial because faster VO2 kinetics
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PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
during a transition to the same work rate will reduce the magnitude of the oxygen deficit, thereby sparing the associated fall
in intramuscular phosphocreatine concentration and attenuating
the production of lactic acid (i.e. allowing the same VO2 to be
attained with less perturbation of the phosphorylation and redox
potentials).
2.5.5
CONCLUSION
As depicted in Figure 2.5.1, an endurance (aerobic) exercise
training session mandates acute circulatory changes that provide
the precise stimulus required to provoke a number of chronic
positive adaptations in cardiovascular function. The changes in
cardiovascular and related parameters that accompany these
adaptations are summarized in Table 2.5.1. At rest and during
submaximal exercise, cardiac output is unchanged after train-
ing; however, a given cardiac output is established via an
increased stroke volume that is attributable to left-ventricular
eccentric hypertrophy, exercise-induced bradycardia, and
increased myocardial contractility. This means that heart rate
and corresponding myocardial work is reduced at any submaximal level of exertion (see Figure 2.5.2). At maximal exercise,
training facilitates a substantial increase in cardiac output that
is exclusively attributable to a greater maximal stroke volume.
This enhancement is mediated by a training-induced increase
in blood volume that facilitates greater venous return, with
central pressure maintained during exercise. Blood vessels are
also altered by training, so that greater flow can be accommodated with less resistance and consequently the time available
for gas exchange with active tissue is increased. As depicted in
Figure 2.5.3, the end result is that the functional capacity of the
cardiovascular system is improved; this is reflected in the ability
to achieve a greater VO2max.
Table 2.5.1 Endurance training-induced cardiovascular adaptations at rest and during
submaximal (same absolute work rate) and maximal exercise
Rest
Submaximal
Maximal
↑
↑
↔
↑
↓
↔↓
↓
↑
↑
↑
↔
↑
↓
↔↓
↓
↑
↑
↑
↔
↑
↔↓
↑
↔
↑
↑
↑
↑
↓
↓
↓
↓
NA
NA
NA
NA
↓
↓
↓
NA
NA
NA
NA
↓
↔↑
↓
↔
↑
↔
↑
↔
↔↑
↔
↔
NA
NA
NA
↓
↑
↔
↔
NA
NA
NA
↔
↑
↑
Cardiovascular adaptations
Myocardial
Venous return
Left-ventricular end diastolic volume
Left-ventricular end systolic volume
Stroke volume
Heart rate
Cardiac output
Rate–pressure product
Coronary blood flow
Peripheral
Plasma volume
Red blood cells
Total blood volume
Haematocrit
Total peripheral resistance
Systolic blood pressure
Diastolic blood pressure
Related
Pulmonary diffusion capacity
Mitochondrial volume/density
Oxidative enzymes (specific activity)
Oxidative enzymes (total activity)
Lipid utilization
Arterio-venous oxygen difference
VO2
c13.indd 174
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CARDIOVASCULAR ADAPTATIONS TO STRENGTH AND CONDITIONING
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2.6 Exercise-induced Muscle Damage
and Delayed-onset Muscle Soreness
(DOMS)
Kazunori Nosaka, Edith Cowan University, School of Exercise, Biomedical and Health Sciences, Joondalup,
WA, Australia
2.6.1
INTRODUCTION
Injurious physical, chemical, or biological stressors damage
skeletal muscles. The severity of muscle damage varies from
micro injury of a small number of muscle fibres to disruption
of a whole muscle, depending on the cause of damage. This
chapter focuses on muscle damage indicated by delayed-onset
muscle soreness (DOMS), which is the most common type of
damage that we experience in our daily life and exercise. It is
predominantly induced by lengthening contractions or isometric contractions at a long muscle length (Clarkson, Nosaka and
Braun, 1992; Jones, Newham and Torgan, 1989). It is also
known that isometric contractions evoked by electrical muscle
stimulation (Aldayel et al., 2009; Jubeau et al., 2008) induce
muscle damage, especially when they are performed for the first
time or a long time after a previous bout.
Here we will describe the characteristics of the muscle
damage induced by eccentric exercise of the elbow flexors.
Although the elbow flexors are often used to study muscle
damage, it should be noted that the muscle damage of the elbow
flexors does not necessarily represent the muscle damage of
other muscles. In resistance training, ‘no pain, no gain’ is often
advocated, therefore we also discuss whether DOMS or muscle
damage is necessary for maximising the effects of resistance
training on muscle hypertrophy and strength gain.
2.6.2
2.6.2.1
SYMPTOMS AND MARKERS
OF MUSCLE DAMAGE
Symptoms
One prominent symptom of muscle damage is sore muscle
developing after exercise (Cheung, Hume and Maxwell, 2003;
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
c14.indd 179
Clarkson, Nosaka and Braun, 1992). As shown in Figure 2.6.1,
other symptoms of muscle damage include muscle weakness,
fatigue, stiff muscle, and muscle swelling (Clarkson, Nosaka
and Braun, 1992; Nosaka, 2008). In order to assess muscle
damage, several direct and indirect markers, including the
measures to quantify the symptoms, are used.
2.6.2.2 Histology
The direct indicator of muscle damage is histological abnormality observed under light (e.g. infiltration of inflammatory cells
to muscle fibres, absence of dystrophin or desmin staining) and/
or electron microscope (e.g. ultrastructural alternation of myofilaments and intermediate filaments) (Fridén and Lieber, 2001;
Gibala et al., 1995; Jones et al., 1986; Stauber and Smith,
1998). To investigate such pathological changes, an invasive
muscle-sampling technique (muscle biopsy) is required; this
can provide only a small amount of muscle tissue, which might
not reflect the muscle damage of a whole muscle.
It should be noted that methodological artefacts could
produce pathological characteristics (Malm, 2001). Raastad
et al. (2010) have reported that 36% of muscle fibres obtained
from muscle biopsy samples show myofiblillar disruptions
characterized by myofillament disorganization and loss of Zdisk integrity following 300 maximal voluntary eccentric contractions of the knee extensors. However, infiltration of
leukocytes in muscle fibres is not seen extensively even after
such exercise, and leucocyte accumulation is primarily in the
endomysium and perimysium (Paulsen et al., 2010). It appears
that the extent of actual histological alternations is minor, even
when sever DOMS is present (Jones et al., 1986; Lieber and
Fridén, 2002).
Crameri et al. (2007) reported that no histological changes
in muscle fibres were observed following 210 maximal
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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Figure 2.6.1 Symptoms, indicators, and measures of exercise-induced muscle damage
voluntary eccentric contractions of the knee extensors, although
severe DOMS occurred and muscle strength was largely
decreased. This suggests that histological abnormality in
muscle fibres is not necessarily associated with DOMS, and
it does not appear that many muscle fibres are actually degenerated following eccentric exercise resulting in DOMS. It has
been documented that ultrastructual changes in muscle fibres
indicate ‘muscle remodelling’ rather than muscle damage (Yu
and Thornell, 2002; Yu, Malm and Thornell, 2002).
2.6.2.3 MRI and B-mode
ultrasound images
Muscle damage can be visualized by magnetic resonance
imaging (MRI) as an increased T2 relaxation time, or by
B-mode ultrasound as an increased echo intensity (Foley
et al., 1999; Nosaka and Clarkson, 1996; Nosaka and
Sakamoto, 2001; Nurenberg et al., 1992). The increased T2
relaxation time is an indicative of increases in water in the
area, probably due to inflammation. It has been shown that
T2 relaxation time increases following eccentric exercise of
the elbow flexors, peaks several days (e.g. six) post-exercise,
and returns to the pre-exercise value in 4–8 weeks (Nosaka
and Clarkson, 1996). As depicted in Figure 2.6.2, the region
showing the increased echo intensity corresponds to the region
showing the increased T2 relaxation time. It is not fully understood what causes the increases in echo intensity, although it
appears to be associated with inflammation (Fujikake, Hart
and Nosaka, 2009).
c14.indd 180
2.6.2.4 Blood markers
Muscle damage is represented by increases in muscle-specific
proteins in the blood such as creatine kinase (CK) and myoglobin
(Mb). When muscle fibres are severely damaged, their plasma
membrane is disrupted and they become necrotic; soluble proteins located in the cytoplasm then leak out from the plasma
membrane and get into the bloodstream. Small proteins can
enter the bloodstream through capillaries, but large proteins
appear to enter via lymph (Lindena et al., 1979). For example,
the molecular weights of CK and Mb are approximately 80 kD
and 18 kD, respectively, and CK reaches the bloodstream via
lymph, while Mb can get in through capillary (Sayers and
Clarkson, 2003). This could explain the delayed increases in
CK activity in the blood, which peaks 4–5 days following
eccentric exercise of the elbow flexors (Figure 2.6.3), while Mb
peaks earlier (e.g. 2–3 days following the eccentric exercise).
The delayed large increases in CK or other enzyme activities
(e.g. aldorase, lactate dehydrogenase, aspartate aminotransferase) in the blood are often seen following eccentric exercise
of limb muscles (Nosaka and Clarkson, 1996). However, these
enzymes already show large increases immediately after endurance events such as marathon or triathlon, and peak 1–2 days
following exercise (Nosaka et al., 2009; Suzuki et al., 2006).
As shown in Figure 2.6.3, structural proteins such as troponin increase in the blood following eccentric exercise of the
elbow flexors. Interestingly, only fast-twitch-type troponin I
increases in a similar way to CK activity. This suggests that
only fast-twitch fibres are damaged in the eccentric exercise.
When the magnitude of CK activity in the blood is small (e.g.
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181
Figure 2.6.2 (a) B-mode ultrasound images of the upper arm taken before (pre), immediately after (post), and four days following eccentric
exercise of the elbow flexors. (b) Magnetic resonance T2 images taken four days post-exercise for two subjects (Subj. H and Subj. K).
1 = triceps brachii, 2 = humerus, 3 = brachialis, 4 = biceps brachii, 5 = subcutaneous fat
Figure 2.6.3 Changes in serum CK activity and serum skeletal
muscle tropinin I concentration for its fast type and slow type before
(pre) and 1–4 days following 210 (35 sets of 6) maximal eccentric
contractions of the elbow flexors performed by eight non-resistancetrained men. From Nosaka et al., unpublished data
<300 IU/l), it may not represent muscle damage, but rather
increased permeability of the plasma membrane, or squeezing
out of CK in the lymph (Nosaka, Sakamoto and Newton,
2002b).
2.6.2.5
Muscle function
A loss of muscle function lasting more than two days is a typical
indicator of muscle damage, and muscle function measures
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such as maximal voluntary contraction strength of any contraction mode are considered to be the best tool for quantifying
muscle damage (Warren, Lowe and Armstrong, 1999). A shift
of optimum angle to a long muscle length has been reported
after eccentric and isometric contractions (Philippou et al.,
2004), and this has been advocated as a sensitive marker of
muscle damage (Proske and Morgan, 2001). In some cases,
muscle strength does not return to the baseline for more than
two months when maximal eccentric exercise of the elbow
flexors is performed by ‘untrained’ individuals (Nosaka and
Clarkson, 1996).
Using electrical muscle and/or nerve stimulation, it is possible to assess contractile property such as twitch torque and
voluntary activation (Prasartwuth et al., 2005, 2006), and give
more information about the causes of strength decrement. It
appears that some central inhibitory mechanisms are associated
with the strength loss after eccentric exercise (Prasartwuth
et al., 2006), but maximal voluntary contraction strength provides a good picture of muscle damage and recovery. If muscle
damage needs to be assessed in practice, a muscle-function
measure in which the presumed ‘damaged’ muscle is involved
(e.g. 1 RM test, jump test) should be performed.
Figure 2.6.4 shows the relationship between the magnitude
of maximal voluntary isometric contractionstrength (MVC) and
peak plasma CK activity. No significant correlation is seen
between the MVC and CK at immediately after exercise, but
the MVC and CK four days post-exercise are highly correlated.
As explained in Section 2.6.2.4, the magnitude of increase in
plasma CK activity is considered to represent the magnitude of
muscle fibre necrosis. Thus, the high correlation seems to indicate that the inability to generate muscle force is associated with
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pre:168°
pre:179°
122°
132°
3 days after
ECC
Figure 2.6.4 Relationship between the level of maximal voluntary
isometric contraction strength (% of pre-exercise level) immediately
after 24 maximal eccentric contractions of the elbow flexors (MVC
@ post) or four days after the exercise (MVC @ d 4) and peak
plasma CK activity. No significant correlation between MVC and CK
was evident for post, but a high correlation is evident for d 4.
Modified from Nosaka et al. (2006)
muscle-fibre damage. Raastad et al. (2010) have recently
reported that the magnitude of decrease in MVC is highly correlated with the number of muscle fibres with myofibrillar disruptions. When muscle strength is affected by muscle damage,
other performance related to muscle function, such as jump
performance (Miyama and Nosaka, 2004), is also affected.
2.6.2.6
Exercise economy
Exercise economy is decreased when muscle damage is present.
For example, Chen et al. (2007b) showed that running economy
during submaximal treadmill running was significantly reduced
for three days following downhill running. Chen et al. (2009b)
reported that significant decreases in running economy during
level running were evident at 80% and 90% VO2peak intensities,
but not at 70% VO2peak. It is possible that the significant effect
of muscle damage on running economy at high intensities (80%
and 90%) reflects the greater number of muscle fibres that
needed to be recruited, along with impairment of the ability to
utilise elastic energy.
2.6.2.7
Range of motion (ROM)
Muscles become stiff with muscle damage (Clarkson, Nosaka
and Braun, 1992; Howell, Chleboun and Conatser, 1993; Jones,
Newham and Clarkson, 1987), and for some muscles this is
reflected in a decrease in range of motion (ROM) around the
joint at which they are located.
Figure 2.6.5 shows a typical elbow joint angle observed after
eccentric exercise of the elbow flexors. The picture on the left
shows the angle when the subject is relaxing so that the arm
hangs down at his side. Before exercise, the angle is 168°, at
c14.indd 182
Relaxed
Extended
Figure 2.6.5 Relaxed and extended elbow joint angles at three days
after 24 maximal eccentric contractions of the elbow flexors
performed by a young man. The relaxed elbow joint was 168° before
the exercise, but decreased to 122°. When he was asked to extend the
elbow joint, he was able to extend to only 132°, although it was 179°
previously
which the elbow joint is nearly straightened. However, the
angle gets smaller following exercise, and generally the largest
decrease is observed at around three days post-exercise. In this
situation, it is not possible for the subject to extend the elbow
joint fully, and as shown in the right-hand picture, the subject
is able to extend the elbow joint only 10° further than the
relaxed angle. Following eccentric exercise of the elbow flexors,
the subjects cannot fully flex the elbow joint angle. Because of
a decrease in the extended elbow joint angle and an increase in
the flexed elbow joint angle, the ROM of the elbow joint
decreases. This can also happen to other joints, but the magnitude of the change does not appear to be as large as that seen
in the elbow joint. Murayama et al. (2000) reported that muscle
becomes harder after eccentric exercise, which could be associated with increases in muscle stiffness.
2.6.2.8 Swelling
Damaged muscles are swollen (Clarkson, Nosaka and Braun,
1992; Howell, Chleboun and Conatser, 1993; Nosaka and
Clarkson, 1996), and this can be detected by an increase in
muscle thickness or volume shown by B-mode ultrasound
(Figure 2.6.4) or MRI, and/or an increase in circumference
(Figure 2.6.6). In Figure 2.6.4, the distance between the subcutaneous fat layer and the humerus is greater at day 4 than before
that point. Figure 2.6.6 shows an arm which performed eccentric exercise of the elbow flexors four days earlier. Compared
to the pre-exercise value, the circumference is more than 40 mm
larger at the upper arm and forearm. The circumference
increases after exercise, but the increase is small (less than 10
mm) immediately after and one-day post-exercise, and peaks
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183
4 days after ECC
Upper arm
48-mm
Forearm
41-mm
Control
Figure 2.6.6 Swelling of the arm observed at four days after 24
maximal eccentric contractions of the elbow flexors performed by a
young man. Compared to the control arm, the exercise arm is bigger,
but their circumferences were similar before exercise. The upper arm
and forearm increased 48 mm and 41 mm, respectively, compared to
pre-exercise value
4–6 days following exercise. Generally, the swelling of the
forearm becomes more conspicuous several days later, because
of the shift of fluid from the upper arm to the forearm due to
gravity.
2.6.2.9
Muscle pain
DOMS is characterized by a sensation of dull, aching pain,
usually felt during movement or palpation of the affected
muscle (Clarkson, Nosaka and Braun, 1992; Miles and Clarkson,
1994). DOMS typically develops several hours after exercise,
peaks at 1–3 days, and disappears by 7–10 days post-exercise
(Cheung et al., 2003). Because of its subjective nature, it is
difficult to quantify the magnitude of muscle pain; however,
several scales, including visual analogue scale (VAS), numerical rating scale, verbal rating scale (VRS), and descriptors differential scale, are often used (Nosaka, 2008).
Two popular scales that have been used in muscle-damage
studies are VAS, which consists of a line (50–100 mm) with ‘no
pain’ at the left and ‘unbearable pain’ at the right, and VRS, in
which descriptors such as ‘no pain’ and ‘unbearable pain’ correspond to numbers (e.g. 1–10). Figure 2.6.7 shows changes in
muscle pain of the biceps brachii on the 100 mm VAS when
the muscle is palpated or extended following 100 maximal
eccentric contractions of the elbow flexors by a middle-aged
man. Muscle pain immediately post-exercise is minimal, but the
pain level increases gradually for the next 48 hours, peaks
between 48 and 60 hours post-exercise, and gradually subsides
by seven days post-exercise. In contrast, Figure 2.6.8 shows
changes in pain of four regions of the body following an ironman triathlon race performed by an experienced triathlete
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Figure 2.6.7 Changes in muscle soreness of a subject (48-year-old,
non-resistance-trained man) evaluated by a 100 mm visual analogue
scale (VAS: 0 = no pain, 100 = extremely painful) for extension of
the elbow joint (extension) and palpating the upper arm before (pre),
immediately after (0), and 6–168 hours after 100 maximal eccentric
contractions (5 sets of 20 repetitions) of the elbow flexors on an
isokinetic dynamometer. From Nosaka, unpublished data
10
Muscle Soreness (0-10 scale)
Exercised
Knee extensors
Knee flexors
Calf
Hip
8
6
4
2
0
pre
2
12
24
36
48
60
72
84
96 108 120
Time (h)
Figure 2.6.8 Changes in muscle soreness of a subject (38-year-old
man, experienced triathlete) evaluated by a Borg scale (0 = no pain,
10 = worst pain imaginable) for palpating knee extensors, knee
flexors, calf and hip muscles before (pre) and 2–120 hours following
an iron-man triathlon race. Modified from Nosaka et al. (2009)
(38-year-old man), described using VRS. The athlete experienced severe muscle pain two hours post-race, and muscle pain
peaked within 12 hours after the race. It is interesting that the
time course of changes in muscle pain is different between different muscles, with the knee extensors showing most longlasting pain, which subsides by five days post-race.
Pain is generally considered a warning signal, but this does
not appear to be the case for DOMS (Nosaka, 2008). Exercise
of sore muscles does not induce additional DOMS and muscle
damage, nor does it retard recovery from the previous eccentric
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exercise bout (Chen and Hsieh, 2001; Nosaka and Newton,
2002a, 2002b). When DOMS is present, moving the sore
muscles attenuates the magnitude of muscle soreness; however,
this effect is temporary and the time course of changes in soreness is not affected (Zainuddin et al., 2006).
2.6.3 RELATIONSHIP BETWEEN
DOMS AND OTHER INDICATORS
It appears that each symptom or marker shows a different aspect
of muscle damage. It is important to note that DOMS does not
represent the time course of muscle damage, and the level of
DOMS is poorly correlated with the magnitude of changes in
other indicators of muscle damage (Nosaka, Newton and Sacco,
2002a; Rodenburg et al., 1993). For example, after maximal
eccentric exercise of the elbow flexors, muscle soreness does
not develop immediately following exercise, but muscle
strength shows its largest decrease at this time point. When
muscle soreness subsides, swelling of the upper arm peaks, and
abnormality in MRI and ultrasound images is greatest around
this time period (Nosaka, 2008).
As shown in Figure 2.6.9, peak muscle soreness assessed by
VAS does not relate to the magnitude of decrease in maximal
voluntary isometric contraction strength and ROM at four days
post-exercise, or to peak plasma CK activity. Severe DOMS
develops with little or no indication of muscle damage, and
severe muscle damage does not necessarily result in severe
DOMS. DOMS does not reflect the magnitude of muscle
damage even within the same individuals. For example, when
the same subjects performed two different intensities of eccentric exercise of the elbow flexors, all of the indirect markers of
muscle damage showed greater changes for maximal intensity
than submaximal intensity; however, no significant differences
in muscle soreness were seen between the exercises (Nosaka
and Newton, 2002c).
It has been documented that connective tissue damage and
inflammation is more responsible for DOMS than muscle-fibre
damage and inflammation (Crameri et al., 2007; Malm, 2001;
Paulsen et al., 2010). Crameri et al. (2007) compared muscle
damage between 210 maximal eccentric contractions with electrical muscle stimulation (EMS) and 210 voluntary maximal
eccentric contractions (VOL) of the knee extensors, and found
that the magnitude of DOMS developed after exercise and the
increase in staining of the intramuscular connective tissue
(tenascin C) were similar between EMS and VOL; however
muscle-fibre damage was evident only after EMS. This suggests
that extracellular matrix (ECM) damage and inflammation
plays a major role in DOMS.
Paulsen et al. (2010) recently reported that the magnitude of
leucocyte accumulation in the endomysium and perimysium
was negatively correlated with the magnitude of DOMS developed after 300 maximal voluntary eccentric contractions of the
knee extensors, and stated that DOMS cannot be explained by
the presence of leukocytes. The cause of DOMS is still not fully
understood.
2.6.4 FACTORS INFLUENCING THE
MAGNITUDE OF MUSCLE DAMAGE
The magnitude of eccentric exercise-induced muscle damage is
influenced by factors such as intensity, number, velocity, and
muscle length of eccentric contractions, as well as training
status and previous use of the muscles in exercise and daily
activities.
Figure 2.6.9 Relationship between peak muscle soreness evaluated by VAS (0 = no pain, 50 = extremely painful) and maximal voluntary
isometric strength at four days post-exercise (% of pre-exercise level), ROM around the elbow joint at four days post-exercise (absolute
difference from the pre-exercise value), and peak plasma CK activity following 24 maximal eccentric contractions of the elbow flexors
performed by 89 non-resistance-trained men. Modified from Nosaka et al. (2002a)
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185
Figure 2.6.10 Changes in muscle soreness, maximal voluntary isometric strength, and plasma CK activity before (pre), immediately after (0),
and 1–5 days after 60 (6 sets of 10) maximal eccentric contractions of the elbow flexors on an isokinetic dynamometer performed by resistancetrained men (Trained) and non-resistance-trained men (Untrained). Modified from Newton et al. (2008)
2.6.4.1
Contraction parameters
The magnitude of muscle damage induced by eccentric exercise
is greater with higher intensity, larger numbers of contractions,
faster velocity, and at longer muscle lengths (Nosaka, 2009).
Chapman et al. (2008a) showed that in 30 eccentric contractions, the effect of velocity was minor, but when 210 eccentric
contractions were performed, the fast-velocity (210 °/s) exercise
resulted in significantly greater changes in most indirect markers
of muscle damage than the slow-velocity (30 °/s) exercise. This
suggests that the number of eccentric contractions is a stronger
predictor of muscle damage, but contraction velocity also
affects the magnitude of muscle damage.
Comparison between two maximal lengthening contraction
regimens in which the elbow joint was extended from 50 to
130 ° (short condition) and from 100 to 180 ° (long condition)
showed that changes in MVC, ROM, upper-arm circumference,
muscle soreness, plasma CK activity, and abnormalities in
B-mode ultrasound and MRI images were significantly greater
for the long condition than the short condition (Nosaka and
Sakamoto, 2001). This was confirmed in the subsequent study
(Nosaka et al., 2005b), in which a short (50–100 °) and a long
(130–180 °) extension range were compared.
2.6.4.2
Training status
The characteristics of muscle damage in trained athletes are different from those of untrained subjects. Newton et al. (2008)
compared trained (performing resistance training at least three
days a week for at least a year) and untrained men for changes
in some indirect markers of muscle damage following 10 sets of
six maximal voluntary eccentric contractions of the elbow
flexors of one arm on an isokinetic dynamometer, which was an
c14.indd 185
unfamiliar exercise for all subjects in both groups. As shown in
Figure 2.6.10, the trained group showed significantly smaller
decreases and faster recovery of maximal voluntary isometric
contraction strength compared with the untrained group. No
significant increases in plasma CK activity were seen in the
trained group, but the untrained group showed large increases.
Interestingly, no significant difference between the groups is
evident for muscle soreness. This is another example where
muscle pain does not reflect the magnitude of muscle-fibre
damage. It should be noted that the muscle strength of the
trained group recovered to the baseline by three days postexercise, when the untrained group showed approximately 40%
lower strength than baseline. These results suggest that
resistance-trained men are less susceptible to muscle damage
induced by maximal eccentric exercise than untrained subjects.
2.6.4.3 Repeated-bout effect
The magnitude of muscle damage from the same exercise bout
is never the same, even for untrained individuals. Compared to
the initial bout of eccentric exercise, a subsequent bout of the
same exercise performed within several weeks results in less
indications of muscle damage. This phenomenon is known as
the ‘repeated-bout effect’ (Clarkson, Nosaka and Braun, 1992;
McHugh, 2003). As depicted in Figure 2.6.11, compared to the
first bout of eccentric exercise of the elbow flexors, a second
bout of the same exercise with the same arm performed four
weeks later resulted in less DOMS, faster recovery of muscle
strength, and smaller increases in plasma CK activity. It has
also been reported that changes in ROM, upper-arm circumference (swelling), B-mode ultrasound and MRI are smaller after
the second bout than after the first (Foley et al., 1999; Nosaka
and Clarkson, 1996). This protective effect is reported to last
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Figure 2.6.11 Changes in muscle soreness, maximal voluntary isometric strength, and plasma CK activity before (pre), immediately after (0),
and 1–4 days after eccentric exercise of the elbow flexors (6 sets of 5 eccentric contractions with a dumbbell) for the first and second (performed
four weeks after the first) bouts by 10 non-resistance-trained men. Modified from Hirose et al. (2004)
for at least several weeks, but the length of the repeated-bout
effect is dependent on markers of muscle damage (Nosaka
et al., 2001a; Nosaka, Newton and Sacco, 2005a).
The initial eccentric bout with minor damage can still
confer some protective effect. It has been reported that performing an initial eccentric bout with a relatively small number
of eccentric contractions produced the repeated-bout effect
(Chen and Nosaka, 2006; Nosaka et al., 2001b), lower-intensity
eccentric contractions (Chen et al., 2007a, 2009b), or eccentric
contractions at short muscle length, which produced minor
muscle damage (Nosaka et al., 2005b). Lavender and Nosaka
(2008a) have shown that a light eccentric exercise which does
not induce changes in any of the indirect markers of muscle
damage confers protection against muscle damage after a more
strenuous eccentric exercise performed two days later. The
greatest adaptation of the muscle against muscle damage is
induced after the first eccentric exercise bout, but some further
protective adaptations are induced in subsequent bouts (Chen
et al., 2009a). This seems to explain the case of the ‘resistancetrained individuals’ shown in Section 2.6.4.2 (Figure 2.6.9).
Using the repeated-bout effect, it is possible to minimize
muscle damage.
2.6.4.4
Muscle
The susceptibility to muscle damage appears to be different
among muscles. Jamurtas et al. (2005) reported that an eccentric exercise of the knee extensors resulted in smaller decreases
and faster recovery of muscle strength, and smaller increases
in plasma CK activity, compared with an eccentric exercise
of the elbow flexors, when the two exercises had the same
number of contractions (6 sets of 12 reps) performed at the
same relative intensity (75% of maximal eccentric torque) using
c14.indd 186
the same subjects (Figure 2.6.12). Interestingly, no significant
difference in DOMS was seen in two exercises. This is another
example where the level of muscle pain does not necessarily
reflect the magnitude of muscle damage. The decreased muscle
damage in the knee extensors seems to be due to the repeatedbout effect.
It has been reported that little muscle damage occurs to the
wrist extensors (Slater et al., 2010). This may be associated
with how much change in muscle length occurs during eccentric
contractions in the range of joint movement.
2.6.4.5 Other factors
Age could be a factor, as shown in animal studies reporting that
old muscles are more susceptible to eccentric exercise-induced
muscle damage than young muscles (e.g. Brooks and Faulkner,
1996). However, this has not been shown clearly in human
studies, at least where voluntary eccentric contractions are performed. For example, a study comparing changes in indirect
markers of muscle damage following eccentric exercise of the
elbow flexors between young and middle-aged (50-year-old)
men did not find significant differences between the groups for
changes in indirect markers of muscle damage, except for
muscle soreness (Lavender and Nosaka, 2008b). This was also
the case for studies comparing young and old (>65-year-old)
men (Chapman et al., 2008b; Lavender and Nosaka, 2006).
Interestingly, muscle soreness is less for the middle-aged and
elderly individuals than for the young (Lavender and Nosaka,
2006, 2008b).
Controversy exists concerning the difference between men
and women for their susceptibility to muscle damage (Nosaka,
2009). It does not appear that gender differences are greater
than individual differences.
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7
5
4
3
2
1
Arm ns
Leg
100
Plasma CK Activity (IU/L)
Muscle Soreness
6
Isometric Strength (% pre)
6000
80
60
Leg
Arm
P<0.05
40
0
pre 1
2
3
4
Time (day)
187
Arm
P<0.05
Leg
5000
4000
3000
2000
1000
0
pre 1
2
3
Time (day)
4
pre 1
2
3
4
Time (day)
Figure 2.6.12 Changes in muscle soreness, maximal voluntary isometric strength, and plasma CK activity before (pre) and 1–4 days after
eccentric exercise of the elbow flexors (Arm) and the knee extensors (Leg) performed by non-resistance-trained men. Modified from Jamurtas
et al. (2005)
2.6.5
MUSCLE DAMAGE
AND TRAINING
Skeletal muscles adapt structurally and physiologically to
mechanical stimuli generated in muscle contractions, and two
common consequences of such adaptations are strength gain
and muscle hypertrophy. The third position stand of the
American College of Sports Medicine on the guidelines for
resistance training (Ratamess et al., 2009) states that both
concentric and eccentric contractions should be included to
maximize muscle hypertrophy. As explained above, eccentric
contractions could induce muscle damage and DOMS.
‘Pain’ occurs during or after training, and some people think
that pain is necessary for a gain in muscle strength and size.
The concept of ‘no pain, no gain’ is popular in sports culture.
This section tries to clarify how much ‘pain’ is necessary for a
‘gain’ in muscle function and muscle volume.
2.6.5.1 The importance of
eccentric contractions
Several studies have reported superiority of eccentric contractions over concentric contractions for muscle hypertrophy. For
example, Higbie et al. (1996) showed that quadriceps crosssectional area increased to a greater extent when training was
eccentric (6.6%) than concentric (5.0%). Hortobagyi et al.
(2000) reported that increases in muscle strength and type II
muscle fibre size after 12 weeks of retraining after 3 weeks of
immobilization were greater for eccentric training than for concentric training. Farthing and Chilibeck (2003) demonstrated
that eccentric training of elbow flexors increased muscle thickness significantly more than concentric training. Furthermore,
c14.indd 187
Vikne et al. (2006) showed that eccentric training (2–3 times a
week over 12 weeks) increased cross-sectional area of the
elbow flexors and their muscle fibres significantly more than
concentric training. One of the reasons why eccentric training
has the potential to induce greater muscle hypertrophy than
concentric training is the higher force generated during eccentric contractions than during concentric contractions (Adams
et al., 2004; Farthing and Chilibeck, 2003). However, it is noted
that concentric training can increases muscle size and strength
in a similar magnitude to eccentric training (Blazevich et al.,
2007). Thus, it does not appear that muscle damage is a prerequisite for muscle hypertrophy.
The rate of protein synthesis is mediated through activations
of protein kinase B (Akt), mammalian target of rapamycin
(mTOR), and p70 S6 kinase (p70s6k), and the Akt/mTOR/p70s6k
pathway is known to be involved in exercise-induced muscle
hypertrophy (Atherton et al., 2005; Bolster et al., 2003).
Eliasson et al. (2006) reported that maximal eccentric contractions of the knee extensors activated p70s6k in the vastus lateralis, but maximal concentric contractions did not, suggesting that
maximal eccentric contractions are more effective than maximal
concentric contractions in stimulating protein synthesis.
Therefore, it seems reasonable to state that eccentric contractions are more potent stimuli than concentric contractions.
2.6.5.2 The possible role of muscle
damage in muscle hypertrophy and
strength gain
Satellite cells, located in the muscle basal laminae, maintain the
myonuclei-to-cytoplasmic volume ratio by adding myonuclei to
the increasing area and length of muscle fibres (Kadi et al.,
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2005), and play a major role in muscle hypertrophy (Adams,
2006). It is known that satellite cells within the injured muscle
fibres are activated to proliferate and differentiate, forming
myoblasts, which can fuse to form myotubes (Quintero et al.,
2009). Thus, it is possible that the activation of satellite cells
by muscle damage will increase hypertrophic responses. In fact,
Crameri et al. (2004) showed that satellite cells were proliferated after a single bout of eccentric exercise of the knee extensors. Since satellite cells are responsible for muscle regeneration,
it seems reasonable to assume that a greater activation of satellite cells will be induced when severe muscle damage is induced.
However, it may be that the satellites cells are used only to
regenerate the necrotic regions of muscle fibres, and are not
necessarily involved in muscle hypertrophy in severe muscle
damage. It should also be noted that protein synthesis should
exceed protein degradation in order for a muscle to be hypertrophied, and muscle damage is the process of protein degradation. If a muscle is damaged regularly, no muscle hypertrophy
will occur. Therefore, damaging muscles does not necessarily
result in muscle hypertrophy, and the benefits of eccentric contractions as a stimulus for muscle hypertrophy should be considered separately from the issue of muscle damage.
2.6.5.3
No pain, no gain?
As explained in the Section 2.6.4.3, muscles become less susceptible to muscle damage when the same or a similar exercise
is repeated. Figure 2.6.13 shows changes in MVC, plasma CK
activity, and muscle soreness when three sets of ten eccentric
contractions of the elbow flexors with a dumbbell of 50% MVC
were performed once a week for eight weeks (Nosaka and
Newton, 2002d). The first training session induced more muscle
damage than the other sessions, and each session resulted in a
large decrease in MVC immediately after exercise, but the preexercise MVC gradually returned to the pre-training level, and
MVC finally returned to the baseline at week 6. Plasma CK
activity increased only after the first training session, indicating
that muscle-fibre damage occurred only after the first session.
Muscle soreness developed following all training sessions, but
the magnitude was smaller following the second to eighth sessions compared with the first session. This may indicate that
some minor connective tissue damage inflammation was
induced in each session. In the study, no muscle hypertrophy
measurement was made, but considering the fact that muscle
hypertrophy is generally evident after several weeks of training,
it seems reasonable to state that muscle damage is not the main
factor for muscle hypertrophy.
The magnitude of the training effect seems to be greater for
eccentric training, possibly due to the greater mechanical stress
of eccentric contractions than of concentric or isometric contractions. It is important to note that eccentric training does not
necessarily induce muscle damage, and muscle is capable of
hypertrophy in the absence of muscle damage. However, some
muscle damage indicators, such as muscle pain and weakness,
are frequently accompanied by resistance training when intending to maximasing mechanical stress to muscles. This is why
some people believe that ‘muscle damage’ is necessary for
muscle hypertrophy and strength gain.
2.6.6
CONCLUSION
DOMS is one of the peculiar symptoms of muscle damage;
however, the magnitude of DOMS does not reflect the magnitude of muscle damage, which can be indicated by the magnitude of loss of muscle strength. The magnitude of muscle
?
Muscle Damage
Muscle Hypertrophy
Protein
Synthesis
Satellite Cell
Activation
Protein
Degradation
Micro Injury
cytoskeleton
myofibers
endomysium
p70s6K
Inflammation
[Ca2+]i Overload
Protease
Activity
mTOR
Mechanical Stress
Figure 2.6.13 Changes in maximal voluntary isometric strength,
plasma CK activity, and muscle soreness (VAS: 0 = no pain,
50 = extremely painful) over eight weeks in which a bout of eccentric
exercise of the elbow flexors (3 sets of 10 eccentric contractions of
the elbow flexors using a dumbbell) was performed once a week.
Modified from Nosaka and Newton (2002d)
c14.indd 188
Akt
Lengthening contractions
+
Figure 2.6.14 Relationship between muscle damage and muscle
hypertrophy. Instead of muscle damage, lengthening contractions
appear to be more potent stimuli for muscle hypertrophy
10/18/2010 5:11:37 PM
CHAPTER 2.6
EXERCISE-INDUCED MUSCLE DAMAGE AND DELAYED-ONSET MUSCLE SORENESS (DOMS)
damage is affected by many factors, such as intensity, volume,
muscle length of eccentric contractions, and individual characteristics such as experience and training. Muscles adapt rapidly
to damaging exercise in order to attenuate the magnitude
of muscle damage. This makes muscles less susceptible to
muscle damage, and when resistance training is progressed, less
muscle damage is induced. Thus, muscle hypertrophy and
c14.indd 189
189
muscle-strength gain in resistance training do not necessarily
relate to muscle damage. However, there is no doubt that eccentric contractions are important for muscle hypertrophy and
muscle-strength gain. It is not muscle damage due to eccentric
contractions but eccentric contractions per se that are responsible for the greater muscle hypertrophy and muscle-strength gain
conferred by eccentric training (Figure 2.6.14).
10/18/2010 5:11:37 PM
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10/18/2010 5:11:37 PM
2.7 Alternative Modalities of Strength
and Conditioning: Electrical Stimulation
and Vibration
Nicola A. Maffiuletti1 and Marco Cardinale2,3, 1 Schulthess Clinic, Neuromuscular Research Laboratory, Zurich,
Switzerland, 2 British Olympic Medical Institute, Institute of Sport Exercise and Health, University College
London, London, UK, 3 University of Aberdeen, School of Medical Sciences, Aberdeen, UK
2.7.1
INTRODUCTION
Recent advancements in technology and the need to develop
innovative alternative solutions to exercise in the last few
years have determined an increase in the use of various
unconventional systems able to stimulate skeletal muscles in
a similar way to conventional resistance exercise. In particular,
electrical stimulation and vibration have been proposed as
alternative forms of exercise for various populations, ranging
from patients in rehabilitation settings to elite athletes trying
to maximize performance. Unfortunately, while research activities are still trying to explain and understand how such
modalities could be used in various populations, there is an
enormous interest in the commercial aspect, which has determined marketing strategies based on overrated and scientifically incorrect claims. The aim of this chapter is to introduce
the reader to such modalities and explain the scientific principles of their applications. We also aim to provide useful
guidelines to help the reader in designing effective programmes
employing electrical stimulation and vibration in various
populations.
2.7.2
Electrical stimulation (ES), which is also called neuromuscular
electrical stimulation, involves artificially activating the muscle,
with a protocol designed to minimize the discomfort associated
with the stimulation. ES has long been used both to supplement
for voluntary muscle activation in many rehabilitation settings,
for example for maintenance of muscle mass and function
during prolonged periods of disuse or immobilization (Lake,
c15.indd 193
1. Does ES training improve muscle strength?
2. Could ES training improve sport performance?
Finally, some recommendations and practical suggestions
for optimizing ES use will be presented.
ELECTRICAL-STIMULATION
EXERCISE
Strength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
1992), particularly for the quadriceps muscle, and to improve
the muscle strength of healthy muscles (Currier and Mann,
1983). More recently, ES has been implemented in competitive
athletes (Delitto et al., 1989).
Typical settings of ES exercise involve the application of
intermittent electrical stimuli (tetani) through surface electrodes, positioned over the muscle motor point, and preprogrammed stimulation units (Figure 2.7.1). Thanks to recent
advances in ES technology, portable battery-powered and relatively low-cost stimulators can be purchased and used by a
growing number of individuals. Therefore, in order to optimize
ES use and minimize the possible risks for the user, it is important to know (1) the main stimulus parameters, (2) how a contraction is triggered by ES, and (3) the acute and chronic effects
of ES use on neuromuscular function.
After a quick overview of the main methodological and
physiological aspects of ES, we will try to answer the following
important questions about the use of ES in sports training:
2.7.2.1 Methodological aspects: ES
parameters and settings
Depending upon the objectives established at the beginning of
the treatment, different ES protocols and parameters can be
used. Besides electrode characteristics (material, size, placement), the main stimulus parameters for ES, which are dictated
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
The dispersive electrodes is
positioned proximally over the
stimulated muscle
Stimulating electrodes are
placed over the muscle motor
points (v. medialis & lateralis)
After a short warm-up, the subject
completes a typical ES strength
training session, which includes
≈30 stimulated contractions of 5-6
seconds, separated by 20-30
seconds of recovery.
ES current amplitude (in mA) is
consistently increased to the
maximal level tolerated by the
subject
The limb is maintained in isometric
conditions so that ES-evoked force
can be expressed as a function of the
MVC force
Frequency: 50-100 Hz
Pulse duration: ≈400 μs
Current amplitude: max tolerated
Evoked force: >30-50% MVC
Figure 2.7.1 Typical settings of ES exercise for the quadriceps muscle
by the physiological characteristics of nerves and muscles,
include:
1. frequency (number of pulses per second)
2. intensity, or current amplitude (which is probably the most
important parameter)
3. pulse characteristics (shape and duration)
4. on/off cycle, or duty cycle (to minimize the occurrence of
fatigue)
5. ramping (to reduce contraction abruptness and improve
comfort).
There is no general consensus on the optimal stimulus
parameters and stimulation conditions (isometric or not), but
there is agreement on some current characteristics. For example,
in order to maximize the level of evoked force (muscle tension),
which is probably the key factor in ES effectiveness (Lieber
and Kelly, 1991), ES strength training should be performed
using pulse rates of 50–100 Hz (Vanderthommen and Duchateau,
2007) and the highest tolerated dose of current (Lake, 1992).
Biphasic symmetrical rectangular pulses lasting 100–500
c15.indd 194
microseconds are commonly adopted. Short (4–6 second)
current bursts are generally separated by rest periods of 20–30
seconds, and the stimulated muscle is maintained in isometric
conditions to control the level of evoked force.
Even though the modulation of ES parameters may facilitate
the effectiveness of this technique, practitioners agree that there
is considerable subject variation in response to ES, and optimization may relate more to the characteristics of the subject than
to the stimulus parameters themselves (Lloyd et al., 1986). In
the same way, Lieber and Kelly (1991) recently suggested that
ES effectiveness would not depend on external controllable
factors (such as electrode size or stimulation current) but rather
on some intrinsic anatomical properties, such as individual
motor nerve branching. We strongly support this notion, and
concur with the idea that ES success is determined, at least in
part, by uncontrollable factors.
2.7.2.2 Physiological aspects: motor
unit recruitment and muscle fatigue
When skeletal muscles are artificially activated by ES, the
involvement of motor units is different from that underlying
10/18/2010 5:11:38 PM
CHAPTER 2.7
ALTERNATIVE MODALITIES OF STRENGTH AND CONDITIONING
voluntary activation. The main argument supporting such a
difference is that large-diameter axons are more easily excited
by electrical stimuli, which will alter the activation order during
ES compared with voluntary contractions (Enoka, 2002).
However, human experiments have yielded contradictory findings, with some studies suggesting preferential or selective
activation of fast motor units with ES, and others demonstrating
minimal or no difference between the two contraction modalities (for an overview of these studies see Gregory and Bickel,
2005). In a recent review paper, Gregory and Bickel (2005)
suggested that motor unit recruitment during ES is non-selective
or random (see also Jubeau et al., 2007); that is, muscle fibres
are recruited without obvious sequencing related to fibre types
(‘disorderly’ recruitment), and therefore ES can be used to
activate fast motor units (in addition to the slow ones) at relatively low force levels. The main differences in motor unit
recruitment between voluntary and stimulated contractions are
summarized in Table 2.7.1.
Table 2.7.1 Motor unit recruitment during voluntary and
ES contractions
Voluntary contraction
Temporal
Spatial
Asynchronous
Dispersed
Rotation is possible
Quasi-complete (even
at the maximum)
Orderly
Yes, selective (slow to
fast)
Consequence
Partially fatiguing
ES contraction
Synchronous
Superficial (close to
the electrodes)
Spatially fixed
Largely incomplete
(even at the
maximum)
No, nonselective/
random (slow
and fast)
Extremely fatiguing
195
The main consequence of such a unique motor unit recruitment pattern for ES is the exaggerated metabolic cost of an
electrically evoked contraction (Vanderthommen et al., 2003),
which, compared to a voluntary action of the same intensity,
provokes greater and earlier muscle fatigue (Theurel et al.,
2007). According to Vanderthommen and Duchateau (2007),
these differences, in motor unit recruitment and thus in metabolic demand between evoked and voluntary contractions, constitute an argument in favour of the combination of these two
modalities of activation in the context of sports training.
2.7.2.3 Does ES training improve
muscle strength?
There is no doubt that it is possible to improve muscle strength
by means of ES training programmes. However, it should be
remembered that ES training-induced strength gains for healthy
muscles are not greater than those that can be achieved with
traditional voluntary training. In a recent systematic review of
ES studies, Bax, Staes and Verhagen (2005) concluded that for
unimpaired quadriceps the effectiveness of ES training is generally lower than with voluntary modalities, while for impaired
(completely or partially immobilized) quadriceps, ES training
could be more effective than voluntary training. This has important implications for the use of ES in the context of post-injury
and/or postoperative rehabilitation. Training studies performed
in the last 20 years have also demonstrated that it is possible to
obtain significant improvements in muscle strength – particularly for the lower-extremity muscles – in amateur and competitive athletes of all levels (Table 2.7.2).
ES training-induced increases in muscle strength are largely
mediated by neural adaptations, for example increased muscle
activation (e.g. Maffiuletti et al., 2002b), particularly in the case
of short-term (3–4 weeks) training programmes. In contrast,
only ES regimens of longer duration (6–8 weeks) can elicit
Table 2.7.2 Applications of ES strength training in competitive sport
Study (year)
Delitto et al. (1989)
Wolf et al. (1989)
Pichon et al. (1995)
Willoughby and Simpson (1996)
Willoughby and Simpson (1998)
Maffiuletti et al. (2000)
Malatesta et al. (2003)
Maffiuletti et al. (2002a)
Brocherie et al. (2005)
Babault et al. (2007)
Maffiuletti et al. (2009)
Sport
Muscle
Weeks (×/wk)
Type of ES: settings;
frequency
Main findings
Weightlifting
Tennis
Swimming
Basketball
Track & field
Basketball
Volleyball
Volleyball
Ice hockey
Rugby
Tennis
Q
Q
LD
BB
Q
Q
Q+CA
Q+CA
Q
Q+CA+G
Q
6 (3)
3 (4)
3 (3)
6 (3)
6 (3)
4 (3)
4 (3)
4 (3)
3 (3)
6 (1–3)
3 (3)
I-LE; 2500 Hz
C-S; 75 Hz
I-OC; 80 Hz
I-PC; 2500 Hz
C/E-LE; 2500 Hz
I-LE; 100 Hz
I-S; 105–120 Hz
I-LE/SC; 120 Hz
I-LE; 85 Hz
I-LE/CM; 100 Hz
I-LE; 85 Hz
↑ weightlifting
↑ strength, sprint, jump
↑ strength, swimming
↑ strength
↑ strength, jump
↑ strength, jump
↑ strength, jump
↑ strength, jump
↑ strength, sprint
↑ strength, jump
↑ strength, sprint, jump
Q: quadriceps; LD: latissimus dorsi; BB: biceps brachii; CA: calf; G: gluteus; I: isometric; LE: leg extension; C: concentric; S: squat; OC: open chain; PC:
preacher curl; E: eccentric; SC: standing calf; CM: calf machine; ↑: significant improvement.
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morphological changes in the muscle (Gondin et al., 2005). In
their well-designed study, Gondin et al. (2005) demonstrated
the time course of neuromuscular adaptations to ES strength
training. After four weeks of training, strength increases were
accompanied by increased muscle activation, while muscle
cross-sectional area was not significantly modified. Interestingly,
both neural and muscular adaptations mediated the strength
improvements observed after eight weeks of ES, which is
similar to the classical model proposed by Sale (1988) for
neuromuscular adaptations to voluntary strength training.
2.7.2.5 Practical suggestions for ES use
2.7.2.4 Could ES training improve
sport performance?
1. warm-up with and without ES
Several studies with individual (e.g. swimming, tennis, trackand-field, weightlifting) and team-sport (e.g. basketball, volleyball, ice hockey, rugby) athletes have reported a significant
improvement in maximal strength, and in some cases even in
anaerobic power production (vertical jump and sprint ability),
after ES training programmes lasting three to six weeks (Table
2.7.2). Despite the lack of scientific evidence, these improvements are likely to affect field performance. However, since the
stress is applied during nonspecific contractions (i.e. isometric
in general), an excessive use of ES could impair motor coordination. Therefore, performance of complex movements requiring high levels of coordination can only be achieved if ES is
used in conjunction with voluntary ‘technical’ exercise, such as
plyometrics (Maffiuletti et al., 2002a). If ES is adequately combined with sport-specific training and logically integrated into
the yearly training season, improvements could be achieved in
the following capabilities:
jumping ability (both general and specific jumps)
sprinting ability (including shuttle sprints)
other sport-related performances (swimming, weightlifting).
As a practical recommendation for both individual and team
sports, it is suggested that ES training could be used to enhance
muscle strength and anaerobic performance without interfering
excessively with sport-specific training; however, it would be
best used early in the training season (i.e. at the beginning of
the preparatory training season).
The main interest of using ES in high-level sport is that
this modality represents a new form of stress from a neuromuscular, metabolic, and also psychological point of view, and
therefore it could be viewed as a new stimulus to favour plasticity. ES could be particularly useful for athletes whose performance has plateaued after several years of training and
competition, but it would be supplementary to, rather than a
substitute for, more traditional forms of training. Another interest of ES for elite sportsmen is that a single ES bout is usually
less time-consuming (12–15 minutes) than traditional volitional
exercise sessions, and this is extremely appealing for athletes
who have a limited amount of time for conditioning (e.g. tennis
players).
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Who should administer ES?
For the first one or two training sessions, ES should be administered by a physical therapist or physical trainer who is familiar
with the methodological and physiological aspects of ES exercise presented here.
How to use ES within a single session
Each ES exercise session should include the following phases:
2. progressive increase in current amplitude to the maximal
tolerated level (5–10 contractions)
3. first series of 10–15 contractions
4. 3–5 minutes of recovery
5. second series of 10–15 contractions
6. cool-down.
Recommendations:
1. Current amplitude should be consistently increased during
the session.
2. Electrode position and joint angle should be modified
between the two series.
3. Whenever possible, both current amplitude (in mA) and
evoked force (as a percentage of the MVC force) should be
controlled to allow ES intensity to be carefully quantified
(Figure 2.7.1).
How to use ES in the context of a
training programme
ES strength-training programmes should be designed as follows:
1. total duration: 2–8 weeks, depending on the objective
2. frequency: 2 then 3 sessions per week
3. volume: 2 then 3 series of 10–15 contractions
4. intensity: current amplitude (and thus evoked force) should
be increased from session to session.
Recommendations:
1. It is desirable to attain an evoked force level of approximately 50% of the MVC force by the end of the first week
of training.
2. Muscle palpation is recommended on a daily basis after the
first few training sessions in order to estimate the degree of
muscle soreness and accordingly adjust training volume/
intensity.
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Caution for acute and chronic use
Athletes are generally reluctant to use this technique as a supplement to training because of the discomfort associated with
artificial activation. Additionally, post-exercise muscle soreness
and damage produced by the electrical current (Jubeau et al.,
2008), particularly in the area beneath the stimulating electrodes, are associated with a high risk of peripheral overreaching/
overtraining (Maffiuletti et al., 2006; Zory, Jubeau and
Maffiuletti, 2010). Despite large inter-individual differences in
the acute and chronic response to ES exercise, these limitations
should be made clear to the end user.
2.7.3
VIBRATION EXERCISE
Before discussing the possibility of implementing vibration in
a training programme it is important to define what characterizes vibration and how it is possible to control its parameters in
training prescription.
Vibration is a mechanical stimulus characterized by an oscillatory motion. The biomechanical parameters determining its
intensity are the frequency and the extent of the oscillation. The
extent of the oscillatory motion can be given as the amplitude
(maximum displacement from equilibrium) or peak-to-peak
displacement (p-to-p D) (the displacement from the lowest to
the highest point). The repetition rate of the cycles of oscillation
determines the frequency (F) of the vibration (measured in
Hertz).
Consequently the magnitude of the vibration stimulus
depends on the amplitude of the oscillations, the frequency, and
the resulting acceleration transmitted to the body, or to parts of
it (see Figures 2.7.2 and 2.7.3). A large number of scientific
studies have been conducted with the aim of investigating the
negative effects of vibrating tools and whole-body vibration
(WBV) on workers exposed to such stimuli for long hours
during their working tasks (Bovenzi, 2002; Cherniack et al.,
Figure 2.7.2 Types of vibration
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197
2008; Griffin, 2004; Mirbod et al., 1999; Pope et al., 2002;
Sanya and Ogwumike, 2005). The possibility of using vibration
as a form of exercise became a novel idea in the 1980s and
1990s thanks to the work of Nazarov (Nazarov and Spivak,
1985) and Issurin (Issurin and Tenenbaum, 1999; Issurin et al.,
1994), who suggested the use of vibrating pulley machines
during strength and flexibility training, and that vibrating
devices be applied directly to the body while the athlete was
performing strengthening exercises. Later on, the use of vibrating plates to allow individuals to perform WBV exercises was
introduced as an effective training modality in elite athletes
(Bosco et al., 1998). Previous work has suggested that vibration
exposure using this and similar modalities elicits small but rapid
changes in muscle length, producing reflex muscle activity in
an attempt to dampen the vibratory waves (Cardinale and
Wakeling, 2005). This reflex muscle activation is likely to be
similar to the tonic vibration reflex (TVR) (Hagbarth et al.,
1976); however, there is currently no firm evidence to suggest
that the neuromuscular responses observed with WBV exercise
are in fact the expression of TVRs. Because muscle spindle
primary endings are most responsive to vibration and thus
responsible for the TVR, most studies have focused on understanding neuromuscular responses to WBV exercise.
Due to the potential for vibration to timulate the neuromuscular system both acutely and chronically, our group introduced
the concept of WBV, hypothesizing the possibility of improving force and power production of the lower limbs by such an
approach (Bosco et al., 1998, 1999a, 1999b; Cardinale and Lim,
2003). Since then, numerous studies have followed, all of which
have tried to analyse and understand how vibration could be
used as a training intervention not only in elite athletes but as
an alternative exercise modality in populations including disabled children (Ward et al., 2004), aged individuals (Bautmans
et al., 2005), and adults with cerebral palsy (Ahlborg et al.,
2006). In recent years, different technologies have been developed to provide vibration-exercise devices similar to typical
gym equipment and/or implementing mechanical and acoustic
vibration modalities (Dessy et al., 2008; Mischi and Kaashoek,
2007; Poston et al., 2007).
There is no current consensus on the effectiveness of vibration exercise in improving force- and power-generating capacity in humans. Some authors are suggesting that there is no
evidence for WBV (Nordlund and Thorstensson, 2007) improving strength and power in the lower limbs; others (in a systematic review of the literature) seem to suggest strong to
moderate evidence for the positive effects of WBV exercise in
untrained people and elderly women (Rehn et al., 2007). A
few more recent reviews of the literature support the suggestion
that vibration exercise could be an effective modality in
improving strength and power of almost all limbs in various
populations (Cardinale and Rittweger, 2006; Cardinale and
Wakeling, 2005; Issurin, 2005; Pavy-Le Traon et al., 2007;
Wilcock et al., 2009).
Despite the clear need for further research, the aggressive
and unscrupulous marketing of many companies has determined the unfortunate appearance of devices which are sold
without proper and safe advice for the user and without any
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Head (axial mode)
(ca. 25 Hz)
Eyeball, intraocular
structures (? 30–80 Hz)
Shoulder
girdle
(4–5 Hz)
Lung
volume
Chest wall
(ca. 60 Hz)
Lower arm
(16–30 Hz)
Hand-arm
Spinal column
laxial model
(10–12 Hz)
Hand grip
(50–200 Hz)
Abdominal
mass (4–8 Hz)
Seated person
Legs
(variable from
ca. 2 Hz with
knees flexing
to over 20 Hz
with rigid posture)
Standing person
Figure 2.7.3 Biodynamic responses to vibration. From Rasmussen (1982)
scientific validation of their safety and effectiveness. This of
course suggests the need for tighter regulatory control over the
production and sale of such devices, which in extreme cases
could result in harmful effects to users. The fitness market is
fundamentally inundated by WBV devices of two types: vibrating platforms which provide a vertical oscillation of the whole
plate, and vibrating platforms with a seesaw movement side-toside of the platform (see Figure 2.7.4). Other vibration exercise
devices include vibrating dumbbells (see Figure 2.7.5), gym
devices capable of transmitting vibration to the user (see Figure
2.7.6), or other vibration exercise tools.
Most of the studies investigating the effectiveness of vibration training have been conducted on non-competitive athletes,
c15.indd 198
sports science students, and/or injured and aged individuals and
special populations. Furthermore, they have largely been conducted using only a few devices, while the market is full of
hundreds that have never been investigated in any wellcontrolled study.
It is very important for the reader to understand that the
effectiveness of vibration exercise is not correlated to the cost
of the device being used, but rather to the correct use of the
effective combination of the key vibration parameters: frequency and amplitude, in combination with appropriate levels
of muscle tension.
Needless to say, devices which provide consistent vibration
parameters and allow such parameters to be unaffected by
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199
Figure 2.7.4 WBV exercise devices
Figure 2.7.5 Vibrating dumbbells
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PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
b)
DAQ (A/D)
PCI-6040E
Motor Drive
a)
Input
Grip
90°
Vibration Motors
PC
30°
AccIn
Interface Board
SCB-68
Pressure
Accelerometer (vibrating plate)
Load cell (vibrating plate)
AccIn
Accelerometer (attached tot user’s limb)
Drive
Lever
Angle
Mechanical
Transmission
Motor
EMG
Goniometer (attached to the user’s leg)
4 Channel Surface EMG System
PC with EMG
Software
DAQ (A/D)
PCI-6220M
Figure 2.7.6 Vibrating gym devices for upper- and lower-body training. (a) Arm flexion/extension device used in Mischi and Cardinale (2009).
(b) Leg press used in Pujari, Neilson and Cardinale (2009) [US Patent No. US7416518 (B2), EU Patent No. EP1524957 (B1)]
the user ’s body mass and the level of force applied is a must,
particular when athletes/users want to perform loaded squatting
exercises on a vibrating platform.
2.7.3.1
Is vibration a natural stimulus?
During all sporting and daily activities our bodies interact with
the external environment and experience externally applied
forces. These forces induce vibrations and oscillations within
the tissues of the body. Tissue vibrations can be induced from
impacts where either a part of the body or an item of sporting
equipment in contact with the body collides with an object.
Impact shocks experienced through the leg when the heel strikes
the ground during each running stride are the most typical
example. Another common one in sport is the impact shock that
occurs when a racquet is used to hit a ball (Elliott et al., 1980;
Hatze, 1992; Li et al., 2004; Timme and Morrison, 2009).
The initial impact causes vibrations within the soft tissues;
after the impact has occurred, the tissues will continue to oscil-
c15.indd 200
late as a free vibration; that is, vibrating at their natural frequency, with the amplitude of these vibrations decaying due to
damping within the tissues. Other examples of tissue vibrations
are those experienced through the legs when skiing or through
the arms when riding on a bicycle. A continuously oscillating
input force drives the soft-tissue vibrations to occur at the same
frequency as the input force, and allows resonance to occur;
however, active damping from muscles can reduce the amplitude of these larger-amplitude vibrations. Therefore, we can
state that we experience soft-tissue vibrations in almost all
sporting activities and the amplitude and frequency of these
vibrations and the ability to cope with them is partly determined
by the natural frequency and damping characteristics of the
tissues.
The body relies on a range of structures and mechanisms in
order to regulate the transmission of impact shocks and vibrations through the body, including bone, cartilage, synovial
fluids, soft tissues, joint kinematics, and muscular activity. The
body is capable of adapting the response to external vibrations
by producing changes in joint kinematics and muscle activity
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ALTERNATIVE MODALITIES OF STRENGTH AND CONDITIONING
which can be controlled on a short time scale. A few recent
studies have suggested that the body has a strategy of ‘tuning’
its muscle activity in order to reduce its soft-tissue vibrations
in an attempt to reduce such deleterious effects (Nigg and
Wakeling, 2001). The muscle-tuning hypothesis predicts that
the level of muscle activity used for a particular movement task
is, to some degree, dependent on the interaction between the
body and the externally applied vibration forces.
A maximally activated muscle can damp free vibrations
so that the tissue oscillations are eliminated after a couple
of cycles (Boyer and Nigg, 2007; Wakeling and Liphardt,
2006). The fact that muscles are actively engaged in damping
vibratory stimuli suggests that exercising with vibratory
stimulation could provide an effective alternative to resistance exercise and improve strength and power capabilities
not only in athletic populations, but in groups which cannot
otherwise perform strength training. Recent work from our
laboratory has shown that neuromuscular activity during
vibration affects agonist and antagonist muscles involved in
the task on which vibration is superimposed, suggesting that
the real benefits of vibration stimulation might appear only
when superimposed on high levels of muscle tension (Mischi
and Cardinale, 2009).
2.7.3.2 Vibration training is not just
about vibrating platforms
Vibration was used in the 1980s mainly by Russian scientists
as an alternative way of improving strength and flexibility in
gymnasts (Nazarov and Spivak, 1985). Recent work from
Mischi (Mischi and Kaashoek, 2007) has shown greater gains
in the use of vibration through combination of vibrating devices
with typical gym strength-training equipment. Applying vibration to barbells has been shown to increase peak and average
power output during bench-pressing exercises (Poston et al.,
2007), while gymnasts have been shown to improve flexibility
using a novel vibrating tool which allows them to perform flexibility training with vibration, suggesting another means of
using vibration as a training stimulus (see Figure 4.4.2) (Sands
et al., 2006). Direct application of vibration to muscles and
tendons has also been suggested to produce acute and chronic
effects in neuromuscular performance and will be discussed
later in this chapter.
2.7.3.3 Acute effects of vibration
in athletes
The acute effects of vibration exercise have been studied mainly
with the aim of identifying the most appropriate combination
of frequency and amplitude to affect strength and power performance. Furthermore, considering the observed effects on
muscle perfusion (Kerschan-Schindl et al., 2001), the interest
in understanding the acute responses to such stimuli is increased
with respect to using vibration as some form of training aid/
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201
warm-up/preconditioning procedure. Few studies have been
conducted using athletes competing in national- and/or
international-level competitions. Bosco et al. (1999b) showed
an acute shift to the right of the force–velocity and power–
velocity relationship in the vibrated leg of elite female volleyball players after 10 sets of 1 minute of static squatting on one
leg performed on a tilting device (F = 26 Hz, p-t-p D = 10 mm),
suggesting the possibility of such modality producing a potentiation effect. Elite female field hockey players were also shown
to increase vertical jumping ability and hamstrings flexibility
after five minutes of WBV (squat) performed on a tilting device
(Novotec, Pforzheim, Germany; F = 26 Hz, p-to-p D = 6 mm).
We have previously suggested that WBV exercise increased
electromyographic (EMG) activity of the leg extensor muscles
in elite female volleyball players by 34% as compared to just
squatting in no-vibration condition (Cardinale and Lim, 2003),
with the peak EMG reached at 30 Hz. For this reason, and due
to the resemblance of such response to the tonic vibration reflex,
we have suggested a ‘muscle tuning’ response aimed at controlling active damping in the soft tissues as one of the mechanisms
leading to the observed performance enhancements (Cardinale
and Wakeling, 2005). This increase in EMG activity has also
been observed by other authors in various populations
(Abercromby et al., 2007; Delecluse et al., 2003; Hazell et al.,
2007; Roelants et al., 2006).
These data need to be also interpreted with caution, as vibration noise can contribute to higher EMG levels and appropriate
filtering techniques will need to be used in future studies to
understand the true contribution of vibration to muscle activation (Abercromby et al., 2007; Fratini et al., 2008; Mischi and
Cardinale, 2009). Short-duration dynamic squatting (30
seconds) performed on a vibrating platform (F = 35 Hz, p-to-p
D = 4 mm) has been suggested to allow college athletes to
produce higher power output during a subsequent squat exercise
with 75% of 1 RM when compared to just resting in between
sets (Rhea and Kenn, 2009). Acute improvements in the ability
to produce force during a plantar flexion task lasting up to eight
minutes have been observed following WBV (F = 30 Hz, p-to-p
D = 3.5 mm) but could not be related to improvement in
motoneural excitability (McBride et al., 2009). Similar results
have been obtained in other studies (Bullock et al., 2008;
McBride et al., 2009). So far, there seems to be a consensus
that some forms of vibration stimulation superimposed on
various levels of muscle activation might increase neuromuscular demands, suggesting the potential of such intervention to
determine acute and chronic effects on force and power
production.
Despite the accepted evidence of higher neuromuscular activation during WBV, the local metabolic demand in leg extensors while performing static squats on a whole-plate oscillating
device (F = 30 Hz, p-to-p D = 4 mm) (Cardinale et al., 2007) as
compared to squatting without vibration does not seem to be
higher; if anything it is actually less after the first 30–40
seconds. However, it seems obvious to suggest that a combination of increases in blood flow, and consequent muscle perfusion (Kerschan-Schindl et al., 2001; Lohman et al., 2007;
Yamada et al., 2005), might acutely favour power production
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due to a consequent increase in muscle temperature (Cochrane
et al., 2008b).
The aforementioned studies show that there is a paucity of
data on elite/well-trained athletes and also that is it very difficult
to recommend specific protocols. However, the following recommendations can be made when using WBV in warm-up or
as a potentiation routine:
1. Frequencies ranging from 20 to 50 Hz seem to be effective.
2. Oscillations ranging from 3 to 10 mm (peak-to-peak D) seem
to be effective.
3. Durations should not be longer than five minutes per set as
they might cause fatigue rather than potentiation.
4. It is preferable if WBV is combined with loaded static and
dynamic exercise to produce the best effects.
5. In order to personalize protocols to each athlete it is important to conduct some simple measurements in order to identify the dose–response relationship to various protocols
(Adams et al., 2009).
Vibrating dumbbells have also shown some promise in
increasing power output acutely due to a large increase in EMG
activity in elite boxers (Bosco et al., 1999a; Issurin and
Tenenbaum, 1999). Recent work has suggested that using a
vibrating dumbbell requires the recruitment of higher-threshold
motor units during an arm flexion task (McBride et al., 2004).
However, no acute gains were observed in climbers using such
a modality of training (Cochrane and Hawke, 2007) and the
potentiation effects were similar to arm-cranking exercise
(Cochrane et al., 2007).
Finally, performing stretching on vibrating devices has been
shown to increase flexibility in gymnasts more than conventional stretching (Sands et al., 2006), and to increase flexibility
without affecting explosive abilities when combined with
stretching (Kinser et al., 2008).
To date, due to the paucity of data of using the dumbbells
and flexibility protocols, it is almost impossible to advise specific protocols. Definitively more studies are needed in this
field, though it is possible to suggest that relatively low frequency ranges (20–40 Hz) and small amplitudes (<5 mm)
should be used to produce maximum gains.
Further applications could see WBV as a recovery modality
(Edge et al., 2009), but more work is needed in this area before
specific guidelines can be provided.
2.7.3.4 Acute effects of vibration
exercise in non-athletes
A wide range of physiological responses to WBV exercise have
been studied so far in non-athletic populations. Aged individuals seem to be able to cope well with five minutes of WBV
exercise and have also been shown to receive some benefits in
the form of acute increases in circulating levels of IGF-1
(Cardinale et al., 2008). The hormonal responses observed in
c15.indd 202
an aged population have been similar to those previously
observed in young healthy individuals (Bosco et al., 2000).
However, recent work does seem to indicate that WBV per se
does not represent a demanding training stimulus able to challenge homoeostasis as measured by hormonal levels in saliva
and/or blood (Cardinale et al., 2006; Di Loreto et al., 2004;
Erskine et al., 2007). A high intensity of neuromuscular activity
has been suggested as the necessary pre-requisite to determine
a marked alteration in hormonal levels, and when WBV is
combined with conventional resistance exercise it seems that
such an intensity could be high enough to trigger training adaptations modulated by hormonal responses (Kvorning et al.,
2006). Various authors have suggested the effectiveness of
WBV exercise in improving force and power production in
various populations with similar protocols (Abercromby et al.,
2007; Cochrane et al., 2008a; Jacobs and Burns, 2009;
Ronnestad, 2009).
Vibrating devices directly applied to the skin of the biceps
brachii (F = 65 Hz, p-to-p D = 1.2 mm) do not seem to provide
any acute benefit to power output (Moran et al., 2007) in an
arm flexion task. And vibration directly applied to the rectus
femoris for prolonged periods (Jackson and Turner, 2003) can
markedly reduce force-generating capacity not only in the limb
where vibration is applied but also in the contralateral limb.
Squatting on a vibrating platform (10 sets × 60 seconds at
26 Hz) seems to be able to acutely reduce arterial stiffness in
healthy men (Otsuki et al., 2008) and affects blood flow, further
suggesting the acute use of vibration exercise as a warm-up
preparation-to-exercise tool in various populations.
2.7.3.5 Chronic programmes of
vibration training in athletes
Regular programmes of vibration training have been studied in
a wide range of subjects, suggesting a lot of benefits. When we
analyse the effectiveness of such programmes in athletes, the
evidence does not seem to be very strong. A five-week training
period characterized by progressive WBV training of frequencies of 35–40 Hz and amplitudes of 1.7–2.5 mm produced no
significant improvements in vertical jumping ability, isometric
and dynamic muscle strength, or maximal knee extension
velocity in well-trained sprinters (Delecluse et al., 2005).
Young elite skiers were shown to benefit from a resistance
exercise programme supplemented by WBV (F = 24–28 Hz,
amplitude 2–4 mm), showing greater improvements in vertical
jumping ability and isokinetic knee and ankle measures than the
resistance exercise-only group (Mahieu et al., 2006). Eight
weeks of WBV training (5 × 40 seconds, with 1 minute rest;
30 Hz, 5 g magnitude) produced a significant improvement in
vertical jumping ability and knee-extensor strength in ballerinas
(Annino et al., 2007).
In our opinion, it is unlikely that vibration exercise alone
using the currently available technologies (vibrating platforms
with frequencies ranging from 10 to 60 Hz and amplitudes
ranging from <1 to 10 mm (peak-to-peak D)) can benefit
athletes. The benefit of such technology would occur only if
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CHAPTER 2.7
ALTERNATIVE MODALITIES OF STRENGTH AND CONDITIONING
resistance exercise could be performed in combination with
vibration stimulation and/or vibration applied to pre-existing
high levels of muscle activation. Preliminary studies in our
laboratory (Pujari, Neilson and Cardinale, 2009) on a novel
patented exercise apparatus (US Patent No. US7416518 (B2)
EU Patent No. EP1524957 (B1), see Figure 2.7.6) characterized
by a vibrating leg press device strongly suggest the superimposition of vibration to specific levels of muscle tension and
muscle actions to obtain maximal gains.
2.7.3.6 Chronic programmes of
vibration training in non-athletes
Various studies have been conducted on the effects of short-,
medium- and long-term programmes of vibration training on
non-athletic populations. Delecluse et al. (2003) have initially
suggested that WBV was superior to resistance exercise in
improving strength of the lower limbs in healthy young women.
It should be noted that the resistance-exercise protocol used by
the resistance-exercise group in this experiment was of relatively low intensity. Roelants et al. (2004a) showed that WBV
produced not only gains in strength but also increases in fat-free
mass in young untrained women, with the effects being similar
in magnitude to those produced by conventional fitness regimes
characterized by a mixture of cardiovascular and strengthtraining activities. Four months of WBV training improved
vertical jump in young men and women but was unable to
improve balance in the same age group (Torvinen et al., 2002).
Eight months with a similar regime improved vertical jumping
activity but did not have an effect on bone density in a young
mixed age group (Torvinen et al., 2003). Young healthy subjects seem to be able to improve strength and power performance if vibration is combined with resistance exercise (Kvorning
et al., 2006), but such improvements are not larger than that
observed with an appropriate conventional resistance-exercise
programme. Chronic low back pain (Rittweger et al., 2002) and
proprioception of the spine (Fontana et al., 2005) seem to
benefit from WBV exercise in untrained populations.
The elderly seem to benefit most from WBV exercise programmes. Numerous studies have in fact suggested that WBV
exercise programmes can be effective in improving strength
and power of the lower limbs in post-menopausal women
(Roelants et al., 2004b; Verschueren et al., 2004). WBV exercise has also been shown to be effective in preventing osteoporosis in aged populations and in young populations with
low bone density (Gilsanz et al., 2006; Gusi et al., 2006;
Iwamoto et al., 2005; Lindqvist, 2003), suggesting such modality as an effective alternative not only to conventional forms
of exercise but potentially also to pharmacological agents for
the prevention of osteoporosis.
2.7.3.7
Applications in rehabilitation
Vibration exercise has the potential of being an effective
alternative and companion to conventional exercise modalities
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203
due to the potential to exercise bed-ridden patients. Recent
studies conducted on bed-rest models have shown the beneficial
effects of resistive exercise combined with vibration in preserving muscle form and function (Bleeker et al., 2005; Blottner
et al., 2006; Mulder et al., 2006, 2007, 2008; Rittweger
et al., 2006). These encouraging results strongly propose the
efficacy of using such a modality in bed-ridden patients and
patients for whom there is the need to preserve and/or restore
muscle form and function. More studies are needed to verify
the efficacy of such a modality on athletes recovering from
various injuries. However, recent results are encouraging.
Proprioception and balance around the knee and ankle joint
seem to be improved following WBV exercise programmes
in injured individuals (Moezy et al., 2008; Trans et al., 2009).
Patients with Parkinson’s disease benefit from WBV exercise,
even if the effects are not superior to conventional physiotherapy and improved balance (Ebersbach et al., 2008). Adults
suffering from cerebral palsy seem to benefit from WBV
exercise (Ahlborg et al., 2006), with improved ability to
produce strength and reduced spasticity and mobility (Semler
et al., 2007). Children and adolescents with osteogenesis
imperfecta also benefit from WBV exercise by improving
muscle strength and mobility (Semler et al., 2008). Spinalcord-injury patients gain benefit from using vibrating dumbbells by improving average power during arm-flexion tasks
(Melchiorri et al., 2007). These results are very encouraging
as vibration could definitively help special populations due
to the simplicity of use of such technology and the costeffectiveness of performing training sessions at home, without
the need for bulky exercise machines. It is important to state
that combinations of various modalities (ES, vibration, and
conventional exercise) should be sought in all cases to make
sure maximum gains are obtained with the least effort in
various populations.
2.7.3.8 Safety considerations
Performing resistance exercise on the currently marketed WBV
plates can be a risky business. First, the surface limits the stance
of the athlete (if squatting is the exercise of choice). Second,
and most importantly, because of the poor manufacturing and
the cheap choice of components, many vibrating plates cannot
sustain heavy loads. In our experience, many commercially
available plates vary frequencies, amplitudes (and hence magnitudes), and directions of vibration in a stochastic manner
when someone tries to perform strengthening exercises on
them.
When using WBV devices it is important to recognize that
body posture and the type of vibrating plate used (Abercromby
et al., 2007) affect transmissibility of vibration to the spine and
the head when exercises are performed standing on the plate.
Lying and/or sitting on the plate should be discouraged as
transmission to the head is quite high and would put the athlete
at risk of spinal degeneration, visual and vestibular damage,
hearing loss, and other health risks (Griffin, 2004). Handheld
vibrating exercise devices and vibrating dumbbells, cables, and
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Higher
Centers
Interneurons
Interneurons
+ α-motoneurons
+ γ-motoneurons –
Spindle
GTO
Efferent signal
Muscle
Mechanoceptors
Stiffness
modulation
Vibrations
Figure 2.7.7 The effects of vibration stimulation on humans. From Cardinale and Bosco 2003
barbells should be used with caution as prolonged use of similar
tools has been linked to degeneration of soft tissues, reduction
in vascularization, and bone and articular damage (Griffin,
2004).
There is a need for more research to fully understand the
potential of using vibratory stimulation to improve strength and
c15.indd 204
power in various populations. However, considering the potential of vibration to stimulate various physiological structures
and modulate muscle function (see Figure 2.7.7; Cardinale and
Bosco, 2003), the aim of future research activities should be to
understand appropriate dose–response relationships to vibration
training.
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ALTERNATIVE MODALITIES OF STRENGTH AND CONDITIONING
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2.8
The Stretch–Shortening Cycle (SSC)
Anthony Blazevich, School of Exercise, Biomedical and Health Sciences, Edith Cowan University, Joondalup,
WA, Australia
2.8.1
INTRODUCTION
Motor tasks requiring high movement speeds or economy are
commonly performed with movement patterns that allow
muscle–tendon units (MTUs) to be stretched before shortening
rapidly, without a significant delay between the two phases.
This is called the stretch–shortening cycle (SSC). Walking,
running, hopping, jumping, stair climbing, throwing, hitting,
and kicking are examples of activities that are typically performed with an SSC. It is well known that the SSC improves
performance by a considerable amount when compared to a
concentric-only movement. For example, vertical jump height
has been shown to be improved by about 8% (Markovic et al.,
2004) and running economy by approximately 50% (Cavagna,
Saibene and Margaria, 1964) through the use of the SSC. In
this chapter, the mechanisms that underpin the performance
enhancement gained through the SSC will be reviewed – in
many cases the relative impact of each mechanism on performance has not been fully elucidated. In addition, some considerations on how to optimize SSC performance are discussed.
2.8.2 MECHANISMS RESPONSIBLE
FOR PERFORMANCE ENHANCEMENT
WITH THE SSC
Elastic energy storage in muscle–
tendon units (MTUs)
There is still some debate as to the mechanisms responsible for
the performance enhancement seen with an SSC. This is partly
because the relative contribution of each mechanism varies as
the force–time characteristics of a movement change. Here, we
will examine the possible role of six elastic and contractile
mechanisms.
2.8.2.1
Elastic mechanisms
Mechanism 1: recovery of elastic
potential energy
In order to understand the role of elastic energy in the enhancement of performance by the SSC, it is important to first underStrength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
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stand some fundamental principles. Many tissues deform
(elongate or compress) when a force is applied to them and can
therefore store elastic potential energy (Figure 2.8.1). The
deformation of a tissue is dependent upon its stiffness and the
force applied to it, according to Hooke’s law: F = kx (Hooke’s
law actually calculates the restoring force rather than the force
required to deform the tissue, so is usually written F = −kx),
where k is the stiffness of the tissue and x is the deformation
distance of the tissue. The equation can be rewritten as k = F/x,
which shows that a stiff tissue requires a high stretching force
(F) to achieve a given stretch or deformation (x). Compliance
is the inverse of stiffness (1/k), so a compliant tissue deforms
easily under a small force.
Most tissues return to shape, or undergo restitution, when
the force that caused the deformation is removed or reduced;
such tissues are called ‘elastic’. Much of the stored energy is
returned as kinetic (movement) energy. The recoil speed of
elastic tissues such as tendons is practically unlimited, so their
shortening can occur at speeds far exceeding those of muscle
shortening. Thus, tissues such as tendons can ensure that MTUs
shorten at speeds exceeding those that use muscle contraction
alone.
Both muscles and tendons can store elastic energy according to
the equation: E = ½ kx2, where E is the energy stored. The
stored energy is thus equal to the area under the force–elongation
curve, as shown in Figure 2.8.1. Muscle–tendon elongation
is the dominant factor influencing energy storage, and this is
reflected by the squared x term in the equation. Although it is
clear that tendons will store energy as they are stretched, it
should be remembered that muscles can store energy as they
are stretched too, particularly over short stretch distances where
cross-bridge cycling does not occur. At all but the longest
muscle lengths this energy is stored in the series elastic components (SECs) within the muscle, including the cross-bridges
and actin and myosin filaments. Studies show that muscle fibres
can be stretched by approximately 3% before cross-bridge
cycling occurs (Flitney and Hirst, 1978), although in pennate
muscles, where fibre rotation occurs as the muscle is stretched,
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
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Figure 2.8.1 The force–length curve for viscoelastic materials, such
as muscle and tendon. An applied force causes stretch in the tissue
(loading). Stiffer tissues stretch less (x) for a given force (F) and
therefore display a steeper curve. The elastic potential energy stored
is equivalent to the area under the loading curve (areas A + B). The
tissue shortens when force is reduced (unloading), but some energy is
dissipated. The energy returned is equal to the area under the
unloading curve (B). The efficiency of elastic energy recovery (%) is
equal to
B − ( A + B)
× 100
(A + B)
the whole muscle may be able to stretch by ∼5%. Thus, a long
muscle such as the vastus lateralis (30–40 cm) can stretch by
1.5–2.0 cm before cross-bridge cycling occurs, which is similar
to the elongation of the Achilles tendon during countermovement jumping (Kurokawa et al., 2003) and hopping (Lichtwark
and Wilson, 2005).
The question therefore arises as to which tissue is most
appropriate for the storage of the energy. The answer lies not
in which tissue can store the most energy, but in the efficiency
and rate with which energy is returned during recoil. Many
studies on human tendon indicate that >85% of the stored
energy can be returned (e.g. Bennett et al., 1986; Pollock and
Shadwick, 1994), although in vivo studies using newly developed ultrasound imaging techniques estimate this to be ∼65–
90% (Lichtwark and Wilson, 2005; Maganaris and Paul, 2000).
Whilst few data exist detailing the efficiency of muscle, one
study on activated rabbit muscle indicates that perhaps only
∼60% of the energy is returned (Best et al., 1994), as the viscous
properties of muscle ensure that energy is converted to heat and
dissipated. These viscous effects also slow the rate of muscle
shortening during recoil, so it is better to store as much energy
as possible in the more efficient tendons in order to optimize
movement performance.
In many SSC actions, muscles are activated to become
highly stiff, and tendon elongation and recoil dominate the
c16.indd 210
Figure 2.8.2 The muscle and tendon undergo shortening and
lengthening at different times in many SSC actions. For example,
research on countermovement jumping (e.g. Kurokawa et al., 2003)
shows that the Achilles tendon–gastrocnemius MTU stays at a
relatively constant length until it shortens rapidly during ankle plantar
flexion (AP) late in the jump sequence. However, the tendon is first
stretched by the active muscles and then recoils at high speed late in
the movement, whereas the muscle shortens slowly during the
movement but remains quasi-isometric late in the movement. Thus,
the high-speed phase of the jump is associated with fast recoil of the
Achilles tendon but minimal shortening of the gastrocnemius muscle
overall muscle–tendon length change. As shown in Figure
2.8.2, this results in the muscle and the tendon operating out of
phase, with tendon recoil providing the greatest shortening
during the high-speed propulsive phase of an SSC movement.
Of course, the influence of tendon recoil versus muscle shortening will be different for the various MTUs within a limb, and
for movements with different force–time characteristics or
movement patterns.
Another question thus arises: how do we ensure that most
of the elastic potential energy is stored in the tendons rather
than the muscles? The answer lies in the fact that when two
springs of different stiffness are placed in series, more energy
is stored in the compliant spring. Therefore, more energy would
be stored in a tendon if its associated muscle were relatively
stiffer. Increases in muscle stiffness can result from both active
and passive mechanisms:
1. Muscles that can produce a large contractile force will resist
lengthening and clearly have a high stiffness (remember,
k = F/x), so increasing a muscle’s size and neural activation
is important (active mechanism).
2. At a given level of muscle force, stretch reflex activation
may increase muscle stiffness during rapid stretch above that
which is developed in the absence of the reflex (Hoffer and
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CHAPTER 2.8
Andreassen, 1981; Sinkjaer et al., 1988) and contributes
within 50 ms of strertch onset (Sinkjaer et al., 1988), so
maximizing facilitatory (e.g. stretch reflex/Ia and II afferents) and minimizing inhibitory (Ib (Golgi), III, IV afferents)
reflex input is important.
3. Muscles that possess stiffer intra-muscular connective tissue
structures (both series and parallel elastic components) will
have a higher passive stiffness (passive mechanism). Little
research has examined intra- and inter-muscular variations
in the stiffness of elastic structures – although, for example,
aponeurosis stiffness is known to vary between muscles and
between individuals (Bojsen-Møller et al., 2004) – and the
influence of force and stiffness in vivo is still unclear.
4. Shorter muscles, or those with shorter fascicles, will have a
higher passive stiffness because compliance (the inverse of
stiffness) increases proportionally with tissue length (passive
mechanism); two springs of the same mechanical properties
placed in series will stretch further than a single spring for
a given force. Indeed, many distal-limb MTUs that store and
release considerable energy in SSC actions have short
muscles attaching to longer tendons (e.g. gastrocnemius–
Achilles tendon complex), which optimizes them for SSC
function.
5. Muscles with greater fluid mass per muscle volume (i.e.
increased turgidity) are stiffer; fluid shifts induced by iondependent osmosis increase muscle stiffness (Grazi, 2008).
Such fluid shifts occur in exercising muscle and may remain
for hours or days after exercise.
6. Muscles, like all viscoelastic materials, will be stiffer when
stretched more rapidly (Lamontagne, Malouin and Richards,
1997; Mutungi and Ranatunga, 1996). Viscous effects are
caused by fluids in the muscle having to flow past intramuscular structures; the more viscous a muscle’s fluid, the more
resistance there is at high stretch speeds.
Thus, interventions that influence these factors might be
expected to influence SSC performance, although in many cases
more research is required to fully understand their relative
impact.
Importance of stored elastic energy in
SSC actions
Although the storage and release of elastic energy is often
considered a primary mechanism affecting SSC performance
(Alexander, 1987), there is some debate as to its true influence
(Bobbert et al., 1996; Voigt et al., 1995). For example, Bobbert
et al. (1996) suggested that the performance enhancement in
countermovement jumping, when compared to squat (static)
jumping, results almost entirely from the increased time for
muscle activation afforded by the countermovement phase (see
Mechanism 3). Nonetheless, other researchers have shown
strong evidence for an important role of elastic energy in countermovement jump performance (e.g. Kawakami et al., 2002;
Kurokawa et al., 2003). A point that might be considered is that
an increase in muscle force is required in order to decelerate in
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THE STRETCH–SHORTENING CYCLE (SSC)
211
the eccentric (downward) phase and then re-accelerate in the
concentric (upward) phase in order to change the body’s
momentum, which will stretch the tendons further. This
increases energy storage and the restoring force applied by the
tendons (e.g. Finni et al., 2003), according to Hooke’s law. By
this reasoning it is not possible for an increase in muscle force
to be the sole contributor to performance enhancement because
the muscle must stretch an elastic tendon. Nonetheless, it could
be argued that the increased restoring force of the tendon is
proportional to the increase in muscle force resulting from the
countermovement, and thus the increased muscle force might
ultimately be responsible for the greater performance.
Regardless, for SSC movements with different force–time
characteristics, it is very likely that the recoil of elastic tissues
contributes to both the velocity and force output of the MTU,
as well as to movement economy. For example, Finni et al.
(2003) showed that in the concentric phase of a drop jump the
stretch and shortening occurred in the quadriceps tendon with
little change in muscle length, whilst in the countermovement
jump there was a greater elongation of the muscle. Subsequently
it was shown that greater intensities of loading (i.e. increases
in force with little or no increase in force production time) in
the eccentric phase of drop-jump tasks increased the stretch–
shortening distance of the vastus lateralis tendon and reduced
that of the muscle, when the height of the jump was held constant (Ishikawa and Komi, 2004; Ishikawa et al., 2006).
Nonetheless, very high loading intensities in the eccentric phase
might result in greater muscle elongation, and thus relatively
less tendon elongation, as the muscle yields under the load
(Ishikawa, Niemelä and Komi, 2005). Thus, the force–time
characteristics of a movement appear to strongly influence the
relative contribution of elastic recoil to velocity and force
production.
With respect to increasing movement speed, it is well known
that muscle power during the concentric phase of an SSC movement far exceeds that which can be produced by even the
fastest muscles. Peak shortening speeds alone might be as fast
as 7–8 fibre lengths/second in fast muscles (Close, 1972), but
force, and thus power (F × v, where v is shortening velocity),
will be low. However, tendons can recoil at very high speeds
and with a large restoring force, so power output can be high.
For example, de Graaf et al. (1987) estimated that 1400 W was
generated by the plantar flexors in a one-leg countermovement
jump. Mammalian limb muscles with a high proportion of
fast-twitch fibres might produce ∼500 W/kg (Brooks, Faulkner
and McCubbrey, 1990; Josephson, 1993); for a plantar flexor
mass of 950 g (based on a muscle density of 1.06 g/ml from
Méndez and Keys, 1960, and a total volume of ∼900 ml per
leg from Fukunaga et al., 1996) the peak power output of
muscle alone would be ∼475 W. This is about a third less of
1400 W reported by Graaf et al. (1987). Ankle power in twolegged countermovement (∼1800 W) and drop jumps (∼2400 W)
also clearly exceeds the capacity of muscle. Although some
other factors might act to augment muscle power in complex
movements, much of this extra power output is thought to
come from the re-use of stored elastic energy. Tendon recoil
increases muscle power output largely because of the high
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PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
recoil speeds; that is, the velocity component of the power
equation (F × v) is improved. Power outputs of MTUs that
exceed those that could be achieved by muscle alone are commonly seen in animal locomotion, so tendons are often referred
to as ‘power amplifiers’.
Power output can also be improved by increasing the force
component of the equation. One limitation of skeletal muscle
is that its ability to develop force decreases with increasing
velocity, according to the force–velocity relationship. In fact,
peak power production is typically produced at shortening
speeds of about 1/3 of maximum, so faster muscle shortening
will inevitably lead to force reduction. However, both modelled
(Hof, van Zandwijk and Bobbert, 2002) and experimental data
(Finni, 2001; Finni, Ikegawa and Komi, 2001; Finni et al.,
2003; Fukashiro and Komi, 1987) show that joint torque and
MTU force at higher velocities are far greater than that predicted by the force–velocity relationship. As shown in Figure
2.8.3, the peak force attained at zero MTU velocity is within
expected limits, but the force produced at higher concentric
speeds is greater than expected. This force enhancement has
been shown to occur without greater muscle activity or an
altered working length of the fascicles (Finni, Ikegawa and
Komi, 2001), so the likely reason for this phenomenon is that
the restoring force of tendon recoil increases the total MTU
force, according to Hooke’s law. At these high MTU shortening
speeds, the muscle itself will often shorten relatively slowly
(see Section 2.8.2.2 and Figure 2.8.2), which allows for a higher
force output than if it were shortening rapidly. The combination
of this higher force and the tendon-restoring force results in a
substantive increase in force at high MTU shortening speeds.
With respect to movement economy, it has long been known
that significant energy savings are achieved through the re-use
of stored elastic energy. In human running for example,
Cavagna, Saibene and Margaria (1964) estimated that around
50% of the energy for running propulsion comes from the
storage and release of elastic energy. This process was suggested to account largely for the efficiency of muscle (actually,
the whole MTU) being increased from ∼0.25 to ∼0.50. This is
because if the deceleration of the body during the early stance
phase were performed only by muscles working eccentrically,
the energy would be lost as heat and muscle work would be
required to re-accelerate the body. But a portion of the kinetic
energy of a body or limb performing a countermovement can
be stored as elastic potential energy and then regained as kinetic
energy in the concentric phase. Recent research suggests that
similar (∼50%) energy savings are made in movements such as
vertical jumping (Bosco, Saggini and Viru, 1997). In fact, in
vivo estimates of energy contributions from individual elastic
tissues are significant, with ∼17% of the energy of running
coming from energy stored in the arch of the foot (Ker et al.,
1987), and ∼16% (Lichtwark and Wilson, 2005) and ∼6%
(Maganaris and Paul, 2002) coming from energy stored in the
Achilles tendon alone during one-legged hopping and walking,
respectively. However, some researchers caution that the
increased economy should not be confused with an increase in
the efficiency of muscle contraction itself, which has been
argued to decrease since some of the work done by the muscle
on the tendon will be lost as heat (e.g. Ettema, 1996; Ingen
Schenau, Bobbert and de Haan, 1997).
2.8.2.2 Contractile mechanisms
While the recovery of elastic potential energy (Mechanism 1)
is a major contributor to the improved force/power production
and economy of many human movements, the storage of this
energy is ultimately dependent on the magnitude of the contractile force that stretches the series elastic components. Five contractile mechanisms (Mechanisms 2–6) are thought to contribute
to the increased contractile force and ultimately to enhanced
performance in SSC actions.
Mechanism 2: force potentiation
Figure 2.8.3 Example data of a force–velocity curve of a distal
MTU measured during an SSC, compared to the force–velocity
relationship for that MTU measured with isokinetic dynamometry
(i.e. concentric-, isometric-, or eccentric-only force recordings
measured at constant angular velocities). During an SSC, the MTU
force rises as it is stretched eccentrically (a), and then falls as the
MTU recoils in the concentric phase (b). The force at some
concentric speeds is higher than that predicted from the force–
velocity curve measured isokinetically (e.g. Finni et al., 2003; Hof,
van Zandwijk and Bobbert, 2002)
c16.indd 212
Although it is typically believed that only factors such as the
length or velocity of a muscle dictate its force-production
capacity, force production also has a history dependence
(Abbott and Aubert, 1952). It is commonly observed that
muscle or fibre force increases by up to twofold when an isometrically contracting muscle is stretched. This substantial
increase is greater at high stretch velocities, but when the stretch
is applied over a constant time period, it is relatively independent of stretch amplitude (Edman, Elzinga and Noble, 1978;
Lombardi and Piazzesi, 1990). Experiments performed on
muscle fibres and whole muscles show that the increase in force
is transient when the stretch is imposed at shorter muscle
lengths (ascending or plateau region of the force–length curve);
that is, it is lost in approximately 20 ms if the muscle is held at
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CHAPTER 2.8
constant length or allowed to shorten. Since many muscles
involved in SSC actions, such as the human gastrocnemius,
typically work on their ascending limb, it has been suggested
that this mechanism is unlikely to be a factor influencing force
production (Brown and Loeb, 2000). However, when stretch is
imposed on muscles at longer lengths (on their descending
limb), the force remains higher compared to an isometric contraction performed at the same muscle length (Edman, Elzinga
and Noble, 1978; Rassier and Herzog, 2004). This increase in
force remains for as long as the muscle is active. One caveat is
that the force enhancement due to stretch is still rapidly lost if
the muscle is allowed to shorten (Edman, Elzinga and Noble,
1978; Herzog and Leonard, 2000), so this mechanism is again
thought not to be responsible for the increases in force observed
when muscles undergo substantial shortening during contraction (e.g. Walshe, Wilson and Ettema, 1998).
Nonetheless, the increase in force of the muscle in the
stretch phase could allow the SEC to store more elastic energy,
and the subsequent drop in force as the muscle shortens provides the necessary conditions for recoil of the SEC (see Section
2.8.3). Also, viscoelastic materials such as muscle increase in
stiffness when stretched rapidly (Mutungi and Ranatunga,
1996). Thus, the rapid stretch of activated muscles in the eccentric phase might ultimately be responsible for some of the
increase in muscle power and efficiency in some SSC actions.
Further research is required to assess the relative importance of
this mechanism for SSC performance.
Mechanism 3: increased time for
muscle activation
Near-maximal muscle force (>90% maximum) typically takes
several hundred milliseconds to develop, although this can vary
between about ∼150 and ∼900 ms depending on the architecture
and voluntary activation rate of the muscle. In many human
movements, the force application phase is considerably shorter
than this (e.g. 100 ms for ground contact in sprint running), so
near-maximal force will not normally be achievable. However,
the concentric phase of an SSC action is preceded by an eccentric, or countermovement, phase where muscle force begins to
increase. Thus, there is a higher level of force prior to the start
of the concentric phase, which increases the amount of work
done (W = F × d, where F is the average force and d is the
distance over which force is produced), as shown in Figure
2.8.4. Bobbert et al. (1996) found that joint moments at the
beginning of the concentric phase of a countermovement jump
were much higher than in the squat jump. Their modelling
indicated that the increase in moment could account for most
of the difference in jump height. This is good evidence that, at
least in some instances such as vertical jump, the increased time
for force development enhances movement performance.
However, several other arguments must be considered. First,
an increase in muscle force will result in a greater elongation
of elastic tissues and hence an increase in elastic energy contribution in the propulsive phase. While this might not always
increase the work done, it can increase the rate of work (power),
as tendon recoil velocity can be much higher than muscle short-
c16.indd 213
THE STRETCH–SHORTENING CYCLE (SSC)
213
Figure 2.8.4 Representative GRF traces from both countermovement
jump (CMJ) and squat (static) jumps (SJ). The higher propulsive force
early in the concentric phase of a CMJ is purported to contribute
substantially to the increased jump height compared to an SJ. This
increased force, and thus work, is shown as area A
ening speeds. So, because greater muscle forces result in greater
tendon stretch, an increased time for activation is unlikely to
ever be a sole contributor. Second, it is likely that SSC actions
performed very rapidly benefit more from the elastic energy
mechanism (Finni et al., 2003; Ishikawa, Finni and Komi,
2003), so the importance of the increased time of activation will
decrease as movement time decreases. In some movements,
such as countermovement jumping on a sledge apparatus, it has
been shown that joint torque measured at the beginning of the
concentric phase is not higher than that obtained in an isometric
contraction at the same joint angle, although there is a greater
joint torque later in the movement (Finni, Ikegawa and Komi,
2001). So the increased time for muscle activation does not
always result in a greater force at the start of the concentric
phase and cannot always be responsible for the increased movement performance. Regardless, the greater time for force development is a likely contributor to greater movement performance
in some SSC movements.
Mechanism 4: pre-load effect
A significant drawback of concentric-only movements is that a
muscle’s ability to develop force is reduced as soon as concentric shortening speed increases, in accordance with the force–
velocity relationship. So a mechanism that allows the muscle
to shorten more slowly (or eccentrically/isometrically) will
result in a higher overall muscle force. Many insects such as
fleas and froghoppers (spittle bugs) use a catch-like mechanism
to prevent joint extension until agonist muscle force is high, so
the concentric phase begins when muscles have already developed high force levels and the elastic tendons are stretched
(Bennet-Clark and Lucey, 1967; Burrows, 2003). Humans use
a countermovement to similar effect. Once a countermovement
is initiated, muscles are activated in order to slow the body or
limb, i.e. to reduce its negative momentum, prior to the concentric phase. This allows muscle force to increase during the
eccentric (countermovement) and isometric (transition) phases
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PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
of the movement, when movement speed is relatively low, so
the concentric phase begins with the muscle already having
developed a high level of force. Thus, the countermovement
preloads the body or limb so that muscle force can be developed
well before the concentric movement speed increases; interestingly, it has been shown that preloading the body using an
eccentric contraction is more beneficial than loading with an
isometric contraction prior to a vertical jump (Walshe, Wilson
and Ettema, 1998), which makes sense given that force potentiation (Mechanism 2) might also be greater when a muscle is
actively stretched.
The result of both an increased time for muscle activation
and this preload effect can be seen in the force traces obtained
during maximal vertical jumps with and without a countermovement (see Figure 2.8.4). It is likely that for some SSC
actions this preload effect, in combination with the greater time
available for force accumulation, substantially improves SSC
performance. However, in other movements such as a repeated
drop-jump exercise (performed on a sledge apparatus; Finni,
2001; Finni, Ikegawa and Komi, 2001) there is clearly no effect
of this mechanism. So other mechanisms must be of greater
importance in some movements.
Mechanism 5: muscle–tendon
interaction (concerted contraction)
A benefit of having tendons that stretch and then recoil during
a movement is that the muscle lengthening and shortening distance can be less for a given joint angle change. This smaller
muscle displacement, also known as concerted contraction
(defined by Hof, Geelen and Berg, (1983) as ‘a contraction in
which the activation is matched to the load to the effect that
the length of the contractile component remains constant’),
allows the sarcomeres to work through shorter ranges and thus
remain closer to their optimum length, should the muscle length
be appropriate for it. Therefore, force production might be
optimized from a force–length perspective. A smaller displacement would also result in a slower shortening speed, and thus
a greater force potential according to the force–velocity relationship. The importance of this mechanism is underlined by
the fact that muscles could not shorten at the speeds required
for many high-speed human tasks, such as sprint running or
jumping, so of course muscle force would be zero under these
conditions. But even in movements where muscles could have
completed the movement without the aid of tendons, the faster
muscle shortening speed would seriously limit maximum force
output. Importantly, isometric muscle contraction requires less
energy per unit force than concentric shortening (Hill, 1938),
so the ability to contract at zero or lower speeds reduces energy
use and increases movement economy. Thus, the ability for
the muscle to contract quasi-isometrically in many SSC activities has a substantial effect on force, power, and movement
economy.
Mechanism 6: reflex contribution
An important role of muscle in SSC actions is to provide sufficient stiffness to allow elastic energy storage in the SEC, and
in particular the tendon. In addition to α-motoneurone activity
c16.indd 214
(Dyhre-Poulsen, Simonsen and Voigt, 1991), reflex activation
(primarily the short-latency, monosynaptic response) is thought
to contribute to muscle stiffness and force (Cordo and Rymer,
1982; Komi, 2003; Voigt, Dyhre-Poulsen and Simonsen, 1998).
The stretch reflex response, resulting from muscle spindle afferent discharge, has been shown to increase muscle force and
joint stiffness (Houk, 1979; Nichols and Houk, 1976). In fact,
Hoffer and Andreassen (1981) showed that a muscle’s resistance to stretch was greater when reflexes were intact than when
they were not, given identical muscle force prior to stretch. This
increased stiffness was not correlated with the amplitude of the
early (presumably monosynaptic) EMG peak, which indicates
a complex, non-activation-dependent influence of the reflex. So
the stretch reflex appears to be an important mechanism for
force application and stiffness regulation in SSC actions.
Nonetheless, there are several arguments against the assertion
that reflexes contribute to SSC performance:
1. The latency of the reflex’s mechanical response (i.e. rise
of force) may be too long to contribute to many SSC
movements.
2. There is considerable evidence that important agonist
muscles may not lengthen during many common SSC
actions, so the stretch reflex cannot be present.
3. The overall increase in muscle activation, measured by the
area under the EMG – time curve, is insufficient to substantially increase muscle force above that resulting from voluntary activation.
Given that these arguments have provided a framework
around which research into the role of the stretch reflex has
progressed, it is probably a good idea to address each in turn.
Latency of the stretch reflex
mechanical response
One of the main concerns regarding the potential importance of
the stretch reflex is that its mechanical response might be too
slow to make a substantial contribution to muscle force or stiffness (e.g. Ingen Schenau, Bobbert and de Haan, 1997). This is
based on the reasonable logic that the fastest stretch reflex
component (the short-latency component) manifests approximately 40 ms after the onset of rapid muscle stretch, and then
the electro-mechanical coupling process takes a further 90–
100 ms (Ingen Schenau et al., 1995; Vos, Harlaar and Ingen
Schenau, 1991). This results in a minimum period of 130 ms
between stretch onset and the resulting rise in force, although
a further delay would be likely as the resulting muscle force is
transferred through compliant tissues such as the tendons to the
skeleton (i.e. there is a moderate rate of force development). By
this argument, an increase in muscle force and stiffness might
only be expected to occur in movements lasting considerably
longer than 130 ms from the onset of stretch (Ingen Schenau,
Bobbert and de Haan, 1997), which rules out human running,
hopping, and bouncing movements. Furthermore, in movements such as countermovement jumping where there is probably sufficient time for the reflex response to impact on
movement performance, the benefit of the SSC has previously
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CHAPTER 2.8
been largely explained by the increase in muscle active state
prior to the concentric phase (Bobbert et al., 1996).
However, experimental evidence is not congruent with this
argument. Nicol and Komi (1998) applied rapid stretches to
the plantar flexor muscles and found a 13–15 ms delay between
the reflex onset and force rise (measured in the Achilles
tendon), giving a total mechanical response time of only
∼55 ms; this response time includes the time required for force
to be transmitted through the elastic components to the skeleton, although it could be considered that there would be an
additional time required for the force to reach sufficient levels
to impact on movement performance. Previous data from
Melvill-Jones and Watt (1971) had already suggested that the
longer-latency stretch reflex response was noticeable after
50–120 ms and was of sufficient time to influence the concentric phases of human hopping, although it was too slow
to influence fast hopping or stepping down from a step. Also,
Ishikawa and Komi (2007) showed that the short-latency stretch
reflex occurred rapidly enough to affect force production in
slow–moderate-speed (2–5 m/s), but not higher-speed (6.5 m/s),
running. Thus, the evidence suggests that the mechanical
response to the stretch reflex has a time course that fits within
the force application times of many, but not the fastest, human
movements.
Do agonist muscles stretch during
SSC actions?
Another assumption that needs to be satisfied is that agonist
muscles are stretched prior to the concentric movement phase.
While it might be assumed that muscles must be stretched in
the eccentric phase of an SSC, it is often the case that the
muscles and tendons work out of phase (as shown in Figure
2.8.2), so muscle stretch–shortening should not be confused
with whole-MTU stretch–shortening. In fact, because of the
substantial compliance of tendons, modelling studies have predicted that the triceps surae (ankle plantar flexors) contract only
isometrically and concentrically in human walking and running,
while the tendon is stretched and recoils over a considerable
range (Hof, van Zandwijk and Bobbert, 2002). Also, some
studies, using ultrasound imaging to visualize the fascicle
shortening–lengthening behaviour of the triceps surae, have not
shown stretch of the fascicles in movements such as walking
(Fukunaga et al., 2001) and running (Lichtwark, Bougoulias
and Wilson, 2007).
However, the recent use of high-frequency ultrasound
video systems has allowed the detection of brief, high-speed
stretches of muscles during some of these SSC movements.
For example, Ishikawa and Komi (2007) showed that the
medial gastrocnemius muscle underwent a brief stretch immediately after foot–ground contact in running at both slow
and fast speeds. These stretches were followed by a detectable short-latency stretch reflex response. In all but the highest
running speeds (6.5 m/s) it was assumed that the reflex was
sufficiently timed to aid force production and improve muscle
stiffness in propulsion. Importantly, fascicle stretch might
also be different in the various muscles within a synergist
group. Sousa et al. (2007) found that the contraction mode
of soleus and gastrocnemius medialis was not the same during
c16.indd 215
THE STRETCH–SHORTENING CYCLE (SSC)
215
different phases of a drop-jump exercise; in fact, soleus
underwent lengthening before shortening over a range of
drop-jump intensities, whereas gastrocnemius tended to shorten
at lower intensities but then to contract either isometrically
or eccentrically in the eccentric (braking) phase of drop
jumps performed at very high intensities. Thus, not only
does fascicle behaviour differ between muscles, but it also
changes according to the force–time characteristics of the
task. Regardless, brief stretch of some muscles can be seen
clearly in human SSC activities when appropriate techniques
are used.
Is the stretch reflex activation of
muscle sufficient to increase muscle
force and stiffness?
One difficulty with ascribing increases in muscle force in SSC
movements to the stretch reflex is that it needs to be shown that
the brief reflex activation could have a substantial effect in
addition to the large muscle activation usually present in these
movements. This is a very difficult thing to do. While it is clear
that the force production from a reflex that is induced in relaxed
muscle is substantial, and easily measured, some researchers
have questioned the potential benefits of stretch reflexes in SSC
actions because the total quantity of EMG measured in the
concentric phase of an SSC action has not been greater than
that of a purely concentric action. For example, Bobbert et al.
(1996) found no increase in EMG amplitude in lower-limb
muscles in a countermovement jump compared to a squat jump,
and Finni, Ikegawa and Komi (2001) found no difference in the
EMG of vastus lateralis in submaximal sledge jumping exercises between SSC and concentric-only conditions. Thus, there
is a question as to the magnitude of the benefit of the reflex
stimulation.
However, novocaine (1%) injections to the motor point of
vastus lateralis, which reduced the stretch reflex response substantially (58–87%) by blocking the gamma efferents to the
muscle spindles, resulted in a significant decrease in countermovement jump height (12.5%) despite no decrease in voluntary (α-motoneurone) activation (Kilani et al., 1989). This is
very good evidence of an important role of (particularly shortlatency, monosynaptic) stretch reflexes. Importantly, Hoffer and
Andreassen (1981) showed that a muscle’s resistance to stretch
was greater when reflexes were intact than when they were
abolished, when muscle force was the same prior to stretch.
Further, Sinkjaer et al., (1988) showed that reflexes in human
dorsiflexor muscles influenced muscle stiffness within 50 ms of
stretch onset and accounted for up to half of the increased stiffness resulting from rapid muscle stretch; reflex contributions to
stiffness were maximal at intermediate levels of voluntary
muscle force. Thus, a stretch reflex appears to be beneficial for
muscle stiffness even if total muscle activation is not noticeably
greater.
Another benefit of the stretch reflex is that it might optimize
the use of the catch-like property of muscles (Burke, Rudomin
and Zajac, 1970), which is an increase in force that occurs when
a brief, high-frequency burst of stimulation, followed by
‘normal’ lower-frequency stimulation, is applied to a muscle.
The high-frequency bursts are associated with increases in
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PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
isometric and dynamic muscle force, with substantial gains
found in some studies. For example, Binder-Macleod and
Barrish (1992) reported a 20% increase in force and 50% reduction in time to a target force when a two-pulse rapid burst was
applied prior to a lower-frequency train of stimulation in rat
soleus muscle. Given that muscles that contribute largely to
SSC movements (e.g. gastrocnemius) work on the ascending
limb of their force–length curve (i.e. at relatively short lengths)
and are required to produce high isometric and concentric
forces during the propulsive phase, it is perhaps important to
note that the potentiating effect of high-frequency bursts is
greater when muscles are at a shorter length (Lee, Gerdom and
Binder-Macleod, 1999; Mela et al., 2002; Sandercock and
Heckman, 1997), are contracting isometrically (Callister,
Reinking and Stuart, 2003; Sandercock and Heckman, 1997) or
concentrically (Binder-Macleod and Lee, 1996; Callister,
Reinking and Stuart, 2003; Sandercock and Heckman, 1997),
and when the muscle force is higher (Lee, Becker and BinderMacleod, 2000). Nonetheless, performance enhancement during
SSC actions has not been explicitly tested, and, although it is
known that variable stimulation influences force production
(Maladen et al., 2007), it has not been determined whether
high-frequency bursts delivered after muscle force has risen
during normal human movements result in a force augmentation. Further research is required to determine whether the
catch-like property of muscle can be exploited during SSC
actions, and whether the brief high-frequency stretch reflex
burst is appropriate to elicit this response.
It should also be remembered that in some SSC movements
the stretch reflex is thought to contribute to a substantial increase
in muscle activity (measured as an increased EMG amplitude)
compared to the concentric-only condition (120–190% increase;
Trimble, Kukulka and Thomas, 2000), although some of this
increase might be associated with the greater time available for
muscle activation and the preload effect of the countermovement phase. Indeed, Trimble, Kukulka and Thomas (2000)
showed that brief high-frequency (100 Hz) nerve stimulations
of the tibial nerve, of magnitudes that would evoke an H- but
not an M-wave response (i.e. reflex, but not direct, muscle
activation), produced negligible EMG activity at rest but significantly increased EMG values when imposed over an MVC.
Thus, the addition of a reflex component appears to be able to
substantially increase activity in contracting muscles. Regardless
of whether an increase in muscle activity is seen, it is likely that
stretch reflexes increase muscle force and stiffness, and therefore SSC performance.
2.8.2.3
Summary of mechanisms
The increase in concentric power output achieved when a rapid
stretch of the MTU precedes it is probably a result of several
mechanisms, which might include the contribution of elastic
energy (i.e. recoil of the SEC), force potentiation from rapid
muscle stretch, an increased time for muscle activation, the
preload effect, force and stiffness augmentation from stretch
reflexes, and a unique interaction between muscle and tendon
c16.indd 216
that allows the muscle to operate at lower shortening speeds
and over shorter distances. There is still considerable doubt over
whether force potentiation can contribute to SSC performance,
although no conclusive data negate the possibility. The relative
contribution of the other mechanisms is debated, although
cumulative evidence suggests that: (1) increased time for activation and preload effects play a more important role in largerrange-of-motion, slower movements such as the vertical jump;
(2) stretch reflexes have their greatest influence in moderateduration tasks such as hopping and slow running; and (3) the
contribution of stored elastic energy increases with (particularly
eccentric) movement speeds, at least until eccentric loading is
great enough to cause the muscle to yield. Clearly, there is a
need for considerable research into the mechanisms of performance enhancement with SSC use.
2.8.3 FORCE UNLOADING: A
REQUIREMENT FOR ELASTIC RECOIL
It is clear that SSC actions involve the storage of elastic energy
in elastic structures, which comes from the kinetic energy of
the countermovement (in jumps, this kinetic energy results from
the gravitational potential energy of the body prior to the jump)
and the work done by the muscles. What is rarely considered
is that, counter-intuitively, elastic energy can only be recovered
when force decreases; it is worth looking at how this happens.
Muscle–tendon forces peak when their shortening velocity
is close to zero, and maximum energy is stored in the tendons.
However, muscle force decreases as movement velocity
increases in the concentric phase, according to the force–
velocity relationship. This allows the tendons to recoil with a
force proportional to their stiffness, according to Hooke’s law
(F = −kx). This high tendon recoil speed allows the muscle to
shorten slower, and thus muscle force can remain higher than
it would have been if it were responsible for the total MTU
shortening. In effect, the rapid shortening of tendons occurs
because the increasing muscle shortening speed ensures that
muscle force decreases.
This mechanism of tendon recoil is assisted by the changing
moment arm about the distal joints (Carrier, Heglund and Earls,
1994; Roberts and Marsh, 2003). At the ankle joint during
hopping, for example, the external moment arm of force is large
(approximately the length of the foot) and the internal moment
arm is small (the distance from the ankle’s joint centre to the
Achilles tendon). In this case there is a large gear ratio, as
shown in Figure 2.8.5. As an example, an external force of, say,
1000 N would create a joint moment of ∼200 Nm. This needs
to be exceeded in order to jump, so the plantar flexor muscles
must produce a force greater than ∼3330 N, based on a moment
arm of 6 cm (Maganaris, Baltzopoulos and Sargeant, 1998).
This large force causes little joint angular acceleration (plantar
flexion) because the joint torque only slightly exceeds the
torque created by the ground-reaction force (GRF). However,
the Achilles tendon is stretched considerably by the muscle
force. As plantar flexion continues, the external moment arm
10/18/2010 5:11:41 PM
CHAPTER 2.8
Figure 2.8.5 The rotation of some joints, such as the ankle (from A
to B in the figure), results in a smaller gear ratio. This is because of
an increase in the internal moment arm (distance from the joint centre
of rotation to the Achilles tendon: r) and a decrease in the external
moment arm (distance from the GRF to the joint centre: R). The
unfavourable gear ratio in A ensures that a large muscle force causes
little joint rotation and maximum tendon elongation, whereas the
favourable gear ratio in B allows a faster muscle shortening speed
and hence results in a decreased muscle force, allowing tendon recoil
to occur
decreases and the internal moment arm increases. Thus, the
relative mechanical advantage of the plantar flexors is increased
(decreased gear ratio) and the larger joint moment results in
substantial joint rotation. The increasing joint angular velocity
necessitates an increase in the muscle shortening speed and
hence muscle force decreases, allowing the tendon to recoil. So
the changing moment arm about the ankle joint provides a
condition for energy storage early in the movement and for
tendon recoil later in the movement. In humans, moment arms
at joints such as the ankle (Maganaris, Baltzopoulos and
Sargeant, 1998) and elbow (Ettema, Styles and Kippers, 1998)
increase with joint extension, which is ideal for optimizing
tendon energy stretch and recoil.
2.8.4
OPTIMUM MTU PROPERTIES
FOR SSC PERFORMANCE
Properties of muscles and tendons that would be optimum for
a muscle–tendon system must vary as the force–time characteristics vary. It is well established that spring-like systems operate
most efficiently when the forces driving them act in resonance
(i.e. at the natural frequency) with the spring. This can be seen
in a simple experiment where a small weight attached to a
spring is perturbed so that is oscillates (Figure 2.8.6): if the
same weight is attached to a stiffer spring, the oscillation frequency will increase; that is, the natural frequency increases
with spring stiffness. Thus, SSC performance will be optimized
c16.indd 217
THE STRETCH–SHORTENING CYCLE (SSC)
217
Figure 2.8.6 The natural frequency of oscillation of a spring system
is a function of the spring stiffness. If the load on the system is the
same, spring A will oscillate slower (longer period of oscillation, T)
than spring B when perturbed. It should also be noted that the
amplitude of oscillation of the stiffer spring (B) will be smaller, but
the rate of energy dissipation (seen as an amplitude reduction) will be
equal. Muscle–tendon systems operate according to the same
principles
when the natural frequency of the MTU system matches the
movement frequency. This principle has been well demonstrated for SSC movements such as the bench-press (Wilson,
Wood and Elliot, 1991b). It follows that movements requiring
large forces to be produced in short time intervals, such as in
the contact phase of sprint running, will likely benefit from
MTUs being relatively stiff, whereas movements requiring
smaller forces to be produced over longer time intervals, such
as a vertical jump, might benefit from MTUs being relatively
compliant. An aim of future research is to develop practical
methods of measuring muscle–tendon stiffness in different
muscle groups and then determining the optima for movements
performed by different individuals and with different force–
time characteristics.
Of course, regardless of the loads imposed on the system,
faster recoil speeds will be realised with stiffer systems since
the acceleration of a mass is dependent on the force applied
(according to Newton’s second law, F = m × a) and the restoring force of a spring increases with spring stiffness (according
to Hooke’s law, F = −kx). The caveat is that a large enough
muscle force must be applied to stretch the stiffer tendon in
order to allow that force to be produced over sufficient time for
acceleration to occur (according to the impulse–momentum
relationship, Ft = Δmv). This might also require a longer activation time since muscle force increases relatively slowly.
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Attention must be given to this because (1) fatigue is increased
as the requirement for force production increases (Kram and
Taylor, 1990) and (2) lower force production, which can be
caused by the fatigue, will lead to reduced energy storage and
a decrease in movement performance. For a sprint runner, the
beneficial effects of an increased recoil speed from a stiffer
MTU might outweigh the increased energy cost, but for other
athletes this will not necessarily be the case. So an optimum
stiffness must be found for each MTU, for each individual, and
for movements with different force–time characteristics.
2.8.5 EFFECTS OF THE TRANSITION
TIME BETWEEN STRETCH AND
SHORTENING ON SSC PERFORMANCE
It is well documented that an SSC action is one in which MTU
lengthening precedes rapid shortening; however, it is also often
considered that a minimum delay between these phases is
essential (e.g. Komi and Gollhofer, 1997). One reason for this
is that imposing a delay between the phases substantially
reduces concentric movement performance (Wilson, Elliot and
Wood, 1991a) and efficiency (Thys, Faraggiana and Margaria,
1972; Henchoz et al., 2006); both performance and efficiency
decay exponentially with time, with a half-life of ∼0.5–0.9 s
(Thys, Faraggiana and Margaria, 1972; Wilson, Elliot and
Wood, 1991a). While the mechanisms underpinning this phenomenon remain to be fully described, it is generally accepted
that two are chiefly at fault: (1) decreased muscle force prior to
the concentric phase; and (2) the dissipation of stored elastic
energy.
The loss of muscle force is probably a consequence of
several factors. First, the reflexes that might be initiated by the
rapid muscle stretch in an SSC have very short response times
(<200 ms), so delaying the concentric phase will limit the
opportunities for the stretch reflex to augment force output.
Second, the preload effect of a countermovement allows a
muscle to build up very large forces, but relatively little force
is required to maintain a posture in the absence of a preload;
for example, it takes less force to hold a squatting position than
to decelerate the body during the countermovement phase of a
vertical jump. So muscle force necessarily drops when a pause
is allowed between the eccentric and concentric phases. The
loss of elastic potential energy is largely a consequence of this
drop in muscle force because: (1) the pause allows for crossbridge cycling to occur, so elastic energy stored is dissipated
as heat; and (2) the decrease in muscle force allows the tendon
c16.indd 218
to shorten and dissipate its energy slowly. Thus, the minimization of the transition time is essential for optimum SSC
performance.
2.8.6
CONCLUSION
SSCs are commonly performed with the aim of improving
movement speed, power, and/or movement economy. SSC
actions are optimized when the natural frequency of the MTU
system matches the movement frequency (i.e. stiffness is
optimized) and when there is minimal delay between eccentric
and concentric forces; however, it should be remembered that
stiffer MTUs provide greater restoring forces and thus faster
recoil speeds, but compliant MTUs store more energy for a
given imposed muscle force. The eccentric, or countermovement, phase provides conditions for greater concentric performance through at least six main mechanisms, whose
contributions vary according to the force–time characteristics
of the SSC movement. Broadly speaking: (1) the contribution
of elastic energy seems to increase with movement speed (i.e.
shorter SSC duration) because total lengthening–shortening
decreases for muscle but increases for tendon; (2) the benefit
of having an increased time for muscle activation is probably
greater for SSC movements with longer durations; (3) the
importance of the preload effect is probably greater when
there is a greater change in momentum between eccentric and
concentric phases; (4) the beneficial effect of the stretch reflex
seems to be greatest in movements of moderate SSC duration
(i.e. it is inconsequential for fast movements lasting less than
∼120 ms and in movements with very low rates of muscle
stretch or slow eccentric–concentric transitions); (5) there is
still debate as to whether the force potentiation phenomenon
contributes to SSC performance, although rapid stretch can
increase muscle force and stiffness because of muscle’s viscous
properties; and (6) the opportunity for muscles to contract
over shorter ranges and at slower speeds contributes significantly to movement economy and (in addition to the restoring
force of the SEC) to an increase in force development at
high MTU shortening speeds, which increases MTU power
production. Although more research is required to understand
the relative importance of these mechanisms, there is probably
an even greater need to develop tests to easily measure MTU
properties (including their stiffness, etc.) and determine which
properties suit SSC movements with specific force–time characteristics. Such tests would provide the practitioner with the
opportunity of optimizing SSC performance in both clinical
and athletic populations.
10/18/2010 5:11:41 PM
CHAPTER 2.8
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2.9
Repeated-sprint Ability (RSA)
David Bishop1 and Olivier Girard2, 1 Institute of Sport, Exercise and Active Living (ISEAL), School of Sport and
Exercise Science, Victoria University Melbourne, Australia, 2 ASPETAR, Qatar Orthopaedic and Sports Medicine
Hospital, Doha, Qatar
2.9.1
INTRODUCTION
High-intensity sprints of short duration, interspersed with brief
recoveries, are common during most team sports (Spencer
et al., 2005). The ability to recover and reproduce performance
in subsequent sprints is therefore important for team-sport athletes and has been termed repeated-sprint ability (RSA). As
RSA has not been strongly correlated with either aerobic power
or anaerobic capacity (Bishop, Lawrence and Spencer, 2003;
Wadley and Le Rossignol, 1998), this suggests that RSA is a
specific quality and that specific tests are required to evaluate
this fitness component (see Chapter 3.3). Tests of RSA predict
both the distance of high-intensity running (>19.8 km/hour) and
the total sprint distance during a professional soccer match
(Rampinini et al., 2007). RSA is therefore a specific fitness
requirement of team-sport athletes and it is important to better
understand the factors which can limit and improve it.
2.9.1.1
Definitions
The main feature of repeated-sprint exercise (RSE) is the alteration of brief, maximal-intensity sprint bouts with periods of
incomplete recovery (consisting of complete rest or low- to
moderate-intensity activity). However, there is potential for
confusion as some authors have also used the word ‘sprint’ to
describe exercise lasting 30 seconds or more (Bogdanis et al.,
1996; Sharp et al., 1986). For the purposes of this chapter, the
definition of ‘sprint’ activity will be limited to brief exercise
bouts, in general ≤10 seconds, where peak intensity (power/
velocity) can be maintained until the end of the entire bout.
Longer-duration, maximal-intensity exercise, where there is a
considerable decrease in performance, will be referred to as
‘all-out’ exercise (Figure 2.9.1).
When sprints are repeated, it is also useful to define two
different types of exercise: intermittent-sprint exercise and
RSE. Intermittent-sprint exercise can be characterized by shortduration sprints (≤10 seconds), interspersed with recovery
periods long enough (60–300 seconds) to allow near-complete
recovery of sprint performance (Balsom et al., 1992a). In comStrength and Conditioning – Biological Principles and Practical Applications
© 2011 John Wiley & Sons, Ltd.
c17.indd 223
parison, RSE is characterized by short-duration sprints (≤10
seconds) interspersed with brief recovery periods (usually ≤60
seconds). The main difference is that during intermittent-sprint
exercise there is little or no performance decrement (Balsom
et al., 1992b; Bishop and Claudius, 2005), whereas during RSE
there is a marked performance decrement (Bishop et al., 2004)
(Figure 2.9.2).
2.9.1.2
Indices of RSA
During RSE, fatigue typically manifests as a decline in maximal
sprint speed (running), or a decrease in peak power or total
work (cycling), over sprint repetitions (Figure 2.9.2). To quantify the amount of fatigue experienced during RSE, researchers
have tended to use one of two terms: the fatigue index (FI)
or the percentage decrement score (Sdec) (Glaister et al., 2008).
These terms are described in more detail in Chapter 3.3. Other
fatigue indices, such as changes in the subsequent maximal
voluntary contraction torque and decreases in the pedalling
rate or moment, have also been used to describe performance
decrement (Billaut, Basset and Falgairette, 2005; Hautier et
al., 2000; Racinais et al., 2007). These fatigue-induced modifications are generally inversely related to the initial sprint
performance (Hamilton et al., 1991; Mendez-Villanueva,
Hamer and Bishop, 2008).
2.9.2
LIMITING FACTORS
The degree of fatigue experienced during RSE is largely influenced by the particulars of the task: the intensity and duration
of each exercise bout, the recovery time between sprint bouts,
the nature of the recovery, the preceding number of highintensity exercise bouts (Glaister, 2005). Other factors such
as time of day (Giacomoni, Billaut and Falgairette, 2006;
Racinais et al., 2005), the sex, age and training status of subjects (Abrantes, Macas and Sampaio, 2004; Ratel et al., 2002,
2005), and whether or not subjects are sickle cell trait carriers
(Connes et al., 2006) also influence the ability to resist fatigue
during RSE.
Marco Cardinale, Rob Newton, and Kazunori Nosaka.
10/21/2010 3:16:46 PM
224
SECTION 2
PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
13
12
Velocity (m/s)
11
10
9
8
7
6
100 m
5
200 m
4
10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180 190 200
Distance (m)
Figure 2.9.1 Sprint profiles of 100 (circle) and 200 m (square) world records for men. The 100 m performance would be defined as a ‘sprint’
exercise, while the 200 m performance would be defined as an ‘all-out’ exercise
2400
Work (J)
2200
2000
Intermittent sprints
1800
Repeated sprints
1600
2.9.2.1 Muscular factors
1400
Muscle excitability
1200
1
2
3
4
Sprint Number
5
Figure 2.9.2 Graph showing the effect of rest duration on maximal
four-second, bicycle-ergometer sprint performance. Intermittent
sprints were performed every two minutes (Bishop and Claudius,
2005), whereas repeated sprints were executed every 30 seconds
(Bishop et al., 2004)
As a consequence of the unpredictable changes that
occur during field testing, most of our knowledge concerning
fatigue-induced adaptations during RSE has been gained from
cycle-based repeated sprinting performed in the laboratory
environment. The strength of this approach is that most of the
influencing variables can be accurately controlled and manipulated. However, the applicability of findings arising from laboratory settings has been questioned (Glaister et al., 2006).
The complex nature of muscle fatigue is also highlighted by
the considerable number of approaches, models, and indices
(see Section 2.9.1) that have been used to account for the
decline in muscular performance. It is now accepted that rather
than a single factor, the decline in performance during RSE
c17.indd 224
might involve changes within the muscle cell itself (muscular
factors) and/or neural adjustments (neuromechanical factors)
(Figure 2.9.3). An improved understanding of the factors precipitating fatigue might allow for the better design of interventions to improve RSE.
At the skeletal muscle level, dramatic changes in transmembrane distribution of Na+ and K+ have been observed following
high-intensity exercise (Allen, Lamb and Westerblad, 2008).
During intense contractions, the Na+–K+ pump cannot readily
reaccumulate the K+ into the muscles cells, inducing up to a
doubling of the extracellular K+ concentration (Clausen et al.,
1998). Such marked cellular K+ efflux may cause muscle membrane depolarization and in turn reduce muscle excitability
(Clausen et al., 1998). By applying an electrical stimulus to
peripheral nerves, the study of the muscle compound action
potential (M-wave) characteristics has been used to determine
whether fatigue alters muscle excitability during multiple-sprint
activities (e.g. tennis; Girard et al., 2008). Decreased M-wave
amplitude, but not duration, was reported after a RSE, suggesting that action potential synaptic transmission, rather than
propagation (impulse-conduction velocity along the sarcolemma), may be impaired during such exercise (Girard et al.,
2007). This suggests that interventions which can increase the
content and/or activity of the Na+–K+ pump may improve RSA.
However, whether a loss of membrane excitability contributes
to muscle fatigue is debatable since a potentiation of the
M-wave response has also been reported following RSE
(Racinais et al., 2007).
10/18/2010 5:11:43 PM
CHAPTER 2.9
REPEATED-SPRINT ABILITY (RSA)
225
Figure 2.9.3 Potential neuromechanical and muscular sites contributing to fatigue
Limitations in energy supply
Phosphocreatine availability
Phosphocreatine (PCr) depletion after maximal sprinting has
been reported to be around 35–55% of resting values (Dawson
et al., 1997; Gaitanos et al., 1993), and the complete recovery
of PCr stores can last more than five minutes (Tomlin and
Wenger, 2001). As recovery times during RSE tests generally
do not exceed 30 seconds, this will lead to only a partial restoration of PCr stores between two successive sprints (Bogdanis
et al., 1996; Dawson et al., 1997). Moreover, these stores will
progressively deplete with the repetition of high-intensity
efforts (Gaitanos et al., 1993; Yoshida and Watari, 1993).
Coupled with the fact that the recovery of power output occurs
in parallel with the resynthesis of PCr, several authors have
proposed that performance during such an exercise mode may
become increasingly limited by PCr availability; that is, there
will be a decrease in the absolute contribution of PCr to the
total ATP production with each subsequent sprint (Bogdanis
et al., 1995; Sahlin et al., 1976) (Figure 2.9.4). In line with this
proposition, strong relationships have been reported between
the percentage of PCr resynthesis and the recovery of performance during repeated, all-out exercise bouts (Bogdanis et al.,
1995, 1996). Thus, performance during multiple-sprint activities may be improved by interventions (training and/or ergogenic aids) that can increase resting concentrations of PCr
stores and/or the rate of PCr resynthesis.
c17.indd 225
Anaerobic glycolysis
Anaerobic glycolysis supplies approximately 40% of the total
energy during a single six-second sprint (Figure 2.9.5) (Boobis,
Williams and Wootton, 1982; Gaitanos et al., 1993). As muscle
glycogen content has been reported to range from 250 to
650 mmol/kg dw, and maximal ATP production from anaerobic
glycolysis is 6–9 mmol ATP/kg dw/s (Hultman and Sjoholm,
1983; Jones et al., 1985; Parolin et al., 1999), this suggests that
normal glycogen stores are unlikely to represent a limiting
factor during RSE, especially as glycogen use decreases with
subsequent sprints (Figure 2.9.6). However, reductions in
dietary carbohydrate intake, and consequently large decreases
in resting muscular glycogen, have been associated with a
greater decline in end-pedalling frequency (last three seconds)
during the last four six-second bouts of an RSE consisting of
15 bouts (Balsom et al., 1999). Thus, the maintenance of appropriate muscle glycogen stores during training (e.g. with a carbohydrate supplementation for subjects on a normal diet)
appears to be important in maximizing RSA (Hultman et al.,
1990). Interventions that are able to increase the contribution
of anaerobic glycolysis during individual sprints may also
improve RSA.
Oxidative metabolism
The contribution of oxidative phosphorylation to the total
energy expenditure during a single short sprint is limited
(<10%; McGawley and Bishop, 2008). As sprints are repeated,
10/18/2010 5:11:43 PM
226
SECTION 2
PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
Figure 2.9.4 Changes in PCr utilization before and after the first and last sprint of a 10 × six-second repeated-sprint test (with 30 seconds of
recovery between sprints) on a cycle ergometer (Gaitanos et al., 1993)
8%
6%
2%
40%
49%
40%
46%
ATP
PCr
Glycolysis
Aerobic
9%
1st sprint
Last sprint
Figure 2.9.5 Changes in metabolism during the first and last sprint of a repeated-sprint exercise (Gaitanos et al., 1993; McGawley and Bishop,
2008; Mendez-Villanueva, Hamer and Bishop, 2007). Note the area of each paragraph represents the total absolute energy used during each sprint
however, aerobic participation increases with time and may
contribute as much as 40% of the total energy supply during
the final repetitions of RSE (McGawley and Bishop, 2008).
This may explain why oxygen availability, which has the potential to influence the magnitude of the aerobic contribution to
ATP resynthesis (work periods) and the rate of PCr resynthesis
(rest periods), has been associated with performance decrements during multiple-sprint activities (Balsom et al., 1994b;
Buchheit et al., 2009; Haseler, Hogan and Richardson, 1999).
In line with this proposition, research has shown that subjects
c17.indd 226
with greater aerobic fitness (Bishop and Edge, 2006) or faster
oxygen uptake (VO2) kinetics (Dupont et al., 2005) have a
superior ability to resist fatigue during RSE. As subjects can
reach their VO2max during the final stage of a RSE (McGawley
and Bishop, 2008), it is not surprising that training (Edge,
Bishop and Goodman, 2005) and ergogenic aids (Balsom,
Ekblom and Sjodin, 1994a) which increase VO2max have also
been found to improve fatigue resistance. Increasing VO2max
may therefore allow for a greater aerobic contribution during
the latter sprints, potentially improving RSA.
10/18/2010 5:11:43 PM
Muscle glycogen (mmol/kg dm)
CHAPTER 2.9
350
Pre
Post
300
250
200
150
100
50
0
1
10
Sprint number
Figure 2.9.6 Muscle glycogen levels before and after the first and
last sprint of a 10 × six-second repeated-sprint test (with 30 seconds
of recovery between sprints) performed on a cycle ergometer
(Gaitanos et al., 1993)
Metabolite accumulation
Acidosis
Historically, it has been proposed that reduced pH (accumulation of H+) in a vigorously contracting muscle, as typically
observed during RSE (Bishop et al., 2004), interferes with the
contractile machinery and/or the rate of glycolytic reactions
(Allen, Lamb and Westerblad, 2008). In support of this suggestion, correlations have been observed between RSA and both
muscle buffer capacity (ßm) and changes in blood pH (Bishop
and Edge, 2006; Bishop et al., 2003, 2004). It has been argued
that the considerable increases in muscle (Bishop and Edge,
2006; Spencer et al., 2008) and blood (Bishop, Lawrence and
Spencer, 2003; Ratel et al., 2005) H+ accumulation may affect
sprinting performance through the inhibition of ATP generation
derived from glycolysis, possibly via negative effects on phosphofructokinase and glycogen phosphorylase enzymes (Spriet
et al., 1989). Thus, repeated-sprint performance may be
improved by interventions that can reduce the accumulation of
H+. At physiological temperatures, however, acidification as a
direct cause of muscle fatigue during RSE has been challenged
for at least three reasons: (1) the time course of the recovery of
force/power following a bout of intense/maximal work is much
faster than that of pH; (2) high power outputs have been
obtained under acidic conditions; (3) the ingestion of sodium
bicarbonate (known to increase extracellular buffering capacity) has, in some cases, no effect on RSE performance (Glaister,
2005). Other studies have even proposed that lactic acid might
preserve muscle excitability (Pedersen et al., 2004), opening
new research avenues to determine whether the link between
acidosis (muscle buffering) and fatigue is just coincidental.
Inorganic phosphate
As a result of rapid breakdown of ATP and PCr during sprinting, there is an increased intramuscular accumulation of Mg2+,
ADP, and inorganic phosphate (Pi), which may in turn impair
RSA. Increasing evidence indicates that at high Pi concentra-
c17.indd 227
REPEATED-SPRINT ABILITY (RSA)
227
tions, there could be a net influx of Pi into the sarcoplasmic
reticulum, which could result in Ca2+–Pi precipitation limiting
Ca2+ available for release (Fryer et al., 1995). In examining
modifications of single-twitch contractile properties pre- to
post-fatigue, RSE-based studies have confirmed that a failure
of the excitation–contraction coupling can occur (Girard
et al., 2007; Racinais et al., 2007). Low-frequency fatigue
(i.e. a decrease in the ratio between mechanical responses to
tetanus at low- and high- frequency stimulations) has also
been detected after run-based repeated sprinting (Girard et al.,
2007), which further suggests that RSA can be improved
through interventions that can limit sarcoplasmic reticulum
dysfunction under fatigue (e.g. reduction of the amount of
free Ca2+ available for release due to Ca2+–Pi precipitation in
the sarcoplasmic reticulum; Allen, Lamb and Westerblad,
2008). However, corroborative scientific evidence for the specific role of Pi in performance decrement during multiple-sprint
activities is far from substantive.
2.9.2.2 Neuromechanical factors
Neural drive
As maximal sprint exercise demands high levels of neural drive,
failure to fully activate the contracting musculature will theoretically decrease force production and therefore reduce
repeated-sprint performance (Ross and Leveritt, 2001). While
not a universal finding (Billaut and Basset, 2007; Girard et al.,
2007; Hautier et al., 2000; Matsuura et al., 2007), a concurrent
decline in sprint performance and the amplitude of EMG signals
(e.g. root mean square and integrated EMG values) has been
reported in several studies (Mendez-Villanueva, Hamer and
Bishop, 2007, 2008; Racinais et al., 2007) (Table 2.9.1). This
suboptimal motor unit activity (i.e. a decrease in recruitment,
firing rate, or both) – which seems to be related to fatigue resistance (Mendez-Villanueva, Hamer and Bishop, 2008) – has also
been highlighted via the MRI technique (Kinugasa et al., 2004)
and interpolated-twitch results have been obtained during postRSE assessment of neuromuscular function (Girard et al., 2007;
Racinais et al., 2007). Such neural adjustments may be caused
by both pre- and post-synaptic inhibitory mechanisms arising
from peripheral receptors (e.g. muscle spindles, Golgi tendon
organs, free endings of group III and IV nerves). Preliminary
evidence, however, suggests that decreases in neural drive
during RSE are not caused by decreases in motoneuron excitability (as assessed by the normalized H-reflex amplitude)
(Girard et al., 2007). In addition, adaptions in neural function
can result in a reduced efficiency in the generation of the motor
command, possibly due to disturbances in brain neurotransmitter (e.g. serotonin, dopamine, acetylcholine) concentration
(Gandevia, 2001). Under this view, it has been suggested that
an increased concentration of free tryptophan (the serotonin
precursor) in the brain, at least during prolonged intermittent
exercise (four hours of tennis singles; Struder et al., 1995), may
reduce the rate of central drive. Although scientific evidence is
lacking, it is likely that ergogenic aids (CHO ingestion), or
training that has the potential to attenuate the rise in the free
10/18/2010 5:11:43 PM
c17.indd 228
Table 2.9.1 A summary of the characteristics and results of studies that have investigated changes in muscle activation parameters during repeated-sprint exercise
Repeated-sprint exercise
Fatigue effects
Study
Subjects
Repetitions
Sprint duration
Recovery duration
Mechanical changes
Billaut and Basset
(2007)
13 PA
10
6s
30 s
Billaut, Basset and
Falgairette (2005)
12 PA
10
6s
30 s
Ì PPO & MPO (∼9–13%) from sp1 to sp8
Ì MVCpost (∼10%)
= MVC+5min (∼−8%) & MVC+10min (∼−6%)
Ì PPO (11%), PR (7%) & PT (14%) from
sp1 to sp10
Hautier et al. (2000)
10 PA
15
5s
25 s
Ì PPO (∼11%), moment produced (∼6%)
& PR (∼5%) from sp1 to sp13
Billaut et al. (2006)
12 PA
10
6s
30 s
Racinais et al.
(2007)
Mendez-Villanueva,
Hamer and
Bishop (2008)
Mendez-Villanueva,
Hamer and
Bishop (2007)
Matsuura et al.
(2006)
9 PA
10
6s
30 s
8 PA
10
6s
30 s
8 PA
10
6s
30 s
Ì PPO (8%, 10 and 11% after sp8, 9,
and 10, respectively)
Ì MVCpost (13%) & MVC+5min (10%)
Ì PPO (∼10%) from sp1 to sp10
Ì MVCpost (16.5%)
Ì PPO & MPO from sp1 to sp5 (∼14 and
∼17%) and from sp1 to sp10 (∼25 and
∼28%), respectively
Ì PPO (∼24%) from sp1 to sp10
Ì TW (∼27%) from sp1 to sp10
8T
10
10 s
35 s
Ì PPO (∼17%) from sp1 to sp10
Matsuura et al.
(2007)
8T
10
10 s
30 s
Ì PPO & MPO (∼25%) after sp8
Giacomoni, Billaut
and Falgairette
(2006)
12 T
10
6s
30 s
Ì PPO (∼10 and 11%), PT (∼2 and 9%) &
TW (∼16%) from sp1 to sp10 in the
morning and evening, respectively
Ì MVCpost (∼15 and 13%) & MVC+5min
(∼10 and 11%) in the morning and
evening, respectively
Muscle activation changes
= VL RMSMVC (∼+10%)
= MFMVC (∼−8%)
= iEMGsprint during RSE
Ì activation time delays (∼90 ms) between VL
and BF EMG onsets from sp1 to sp10
Ì RMSsprint in BF and GL (∼13 and 17%) from
sp1 to sp13
= RMSsprint in GM, VL and RF from sp1 to sp13
Ê VL RMSMVC (∼15%) post-RSE
= VM RMSMVC (∼+10%) post-RSE
Ì VL and VM MFMVC (∼15%) post-RSE
Ì VL RMSsprint (∼14%)
Ì VL RMS/MMVC (14.5%) & VA (2.5%)
Ì VL RMSsprint from s1 to s5 (∼9%) and from
sp1 to sp10 (∼14%)
Ì VL RMSsprint (∼14%) from s1 to s10
Ì VL MFsprint (∼11%) from s1 to s10
Ì VL and RF iEMGsprint (∼12–15 and 20%)
from sp1 to sp10
= VL and RF MPFsprint from s1 to s10
= VL RMSsprint during RSE
Ì VL MPFsprint (∼5–10%) after sp3 and sp7
only
Ê VL RMSMVC (∼7.5 and 10% in the morning
and evening) after RSE
10/18/2010 5:11:43 PM
Ì, decrease; Ê, increase; =, no significant change; PA, physically active; T, trained; RSE, repeated-sprint exercise; sp1, sprint 1. PPO, peak power output; MPO, mean power output; MVC, maximal voluntary
contraction torque; PR, maximal pedalling rate; PT, peak torque applied on the crank; TW, total work.
RMS, root mean square; RMS/M, normalized RMS activity; iEMG, integrated EMG; MF, median frequency; MPF, mean power frequency; MVC+5min, MVC torque measured +5min after RSE; RMSsprint, RMS
measured during sprinting; RMSMVC, RMS measured during MVC; VA, voluntary activation. VL, vastus lateralis; VM, vastus medialis; RF, rectus femoris; BF, biceps femoris; GL, gastrocnemius lateralis; GM,
gluteus maximus.
All data were collected during cycle-based repeated-sprinting protocols using a passive recovery mode between exercise bouts.
CHAPTER 2.9
REPEATED-SPRINT ABILITY (RSA)
229
tryptophan-branched-chain amino acids ratio in the circulation
(by lowering the free fatty acid levels during exercise), could
theoretically improve repeated-exercise performance. Further
studies are needed to better understand the role of decreases in
neural drive (and the mechanisms of these adaptations) on the
aetiology of muscle fatigue during RSE.
finding may support the view that the ability to maintain a
high-level stiffness condition improves fatigue resistance
during RSE. As joint-stiffness regulation has been related to a
subject’s fitness level (Clark, 2008), this provides another
mechanism by which improving aerobic fitness may improve
RSE-based performance.
Muscle recruitment strategies
Homoeostatic perturbations affecting
fatigue resistance
Billaut, Basset and Falgairette (2005) have reported that the
time delay between the knee extensor and the flexor EMG
activation onsets was reduced during the last sprint of an RSE,
owing to an earlier antagonist activation with fatigue occurrence. Using fifteen 5-second cycle sprints separated by 25
seconds of recovery, Hautier et al. (2000) observed a significant
reduction in RMS for the knee flexor muscles in the thirteenth
compared to the first sprint, without changes in the knee extensor muscles, highlighting a possible decrease in muscle coactivation with fatigue. In addition, a shift of median frequency
values (obtained during MVC) toward lower frequencies has
been reported during post-RSE tests (Billaut et al., 2006). This
has been interpreted as a modification in the pattern of muscle
fibre recruitment and a decrease in the conduction velocity of
active fibres. More tellingly, it is probable that the relative
contribution of type I muscle fibres involved in force generation
increases during RSE protocols as a result of the greater fatigability of type II fibres, highly solicited during this exercise mode
(Casey et al., 1996). Matsuura et al. (2006) added further
support to this notion by showing that during cycle-based
repeated sprinting, mean power frequency is lower with 35second compared with 350-second recovery periods. This
would ultimately suggest that greater fatigue is linked to a
preferential recruitment of slow-twitch motor units. Thus, training that can attenuate or delay the fast-to-slow shift in muscle
fibre recruitment that occurs with fatigue could potentially
improve repeated-sprint performance.
Stiffness regulation
Although not as extensively studied (Ross and Leveritt, 2001),
changes in mechanical behaviour (stiffness regulation) may
also contribute to performance decrements during maximal
efforts such as sprinting. It is generally believed that a stiffer
system allows for more efficient elastic energy contribution,
potentially enhancing force production during the concentric
phase of the movement (Farley et al., 1991). Supported by the
close relationship between leg stiffness and sprint performance
(Chelly and Denis, 2001), it has been argued that stiffness
regulation is a vital component of setting stride frequency
(Farley et al., 1991). In line with this statement, decreased
stride frequencies have been shown to accompany fatigue
development during run-based repeated sprinting (Buchheit
et al., 2009; Ratel et al., 2005). Although stiffness has never
been systematically calculated during each sprint repetition of
an RSE, it is interesting to note that impairment in the springmass model properties of the runner ’s lower limbs (e.g. vertical
stiffness) and performance decrement induced by the repetition
of all-out efforts (four × 100 m interspersed with two minutes
of recovery) have been correlated (Morin et al., 2006). This
c17.indd 229
Fatigue resistance is likely to be compromised as a result
of several homoeostatic perturbations, for example hypoxia,
hyperthermia, dehydration, low glycogen concentration, a
reduced cerebral function (decreased neurotransmitter concentration), and/or the occurrence of muscular damage.
Investigating how hyperthermia affects repeated-sprint performance, Drust et al. (2005) have reported that the ability to
produce power during such an exercise mode is impaired when
core and muscle temperatures are simultaneously elevated. In
the absence of metabolic changes (muscle lactate, extracellular
potassium), these authors have associated the reduced performance in heat with the negative influence of high core temperature on the function of the central nervous system (e.g. alterations
in brain activity, reductions in cerebral blood flow, increases in
whole-brain energy turnover, reduced muscle activation). While
more research is required to establish the mechanisms of these
responses, interventions that can mitigate the development of
homoeostatic-induced perturbations during RSE may improve
fatigue resistance in hostile conditions (see Section 2.9.3).
2.9.2.3 Summary
The inability to reproduce performance in subsequent sprints
(fatigue) during RSE is manifested by a decline in sprint speed
or peak/mean power output. Proposed factors responsible for
these performance decrements include limitations in energy
supply, metabolic byproduct accumulation (e.g. Pi, H+), and
reduced excitation of the sarcolemma (increases in extracellular
K+). Although not as extensively studied, failure to fully activate the contracting muscle may also limit repeated-sprint performance. Moreover, the details of a task (e.g. changes in the
nature of the work/recovery bouts) will determine the relative
contribution of the underlying mechanisms (task dependency)
to fatigue. Additional homoeostatic perturbations (e.g. hypoglycaemia, muscle damage, hyperthermia) are likely to further
compromise fatigue resistance during RSE. Interventions (e.g.
ergogenic aids or training) which are able to ameliorate the
influence of these limiting factors should improve RSA.
2.9.3
ERGOGENIC AIDS AND RSA
The use of ergogenic aids provides a valuable means of experimentally assessing and confirming the possible determinants of
fatigue during repeated-sprint tasks (see Section 2.9.2). The
term ‘ergogenic’ is derived from the Greek words ergon (work)
and gennan (to produce). Hence, an ergogenic aid usually refers
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PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
to something that enhances work. With such a broad definition,
ergogenic aids could include nutritional aids (e.g. supplements),
physiological aids (e.g. training or taper techniques), psychological aids (e.g. imagery), and biochemical aids (e.g. factors
that modify technique). For the purpose of this chapter, the
discussion of ergogenic aids that can improve repeated-sprint
performance will be limited to ingestible substances.
Furthermore, this chapter will only discuss substances that are
not currently banned by the International Olympic Committee
(IOC). While the legal implications regarding the use of ergogenic aids are generally well defined, the moral/ethical implications are less clear. The following section is concerned with
how ergogenic aids can help us better understand the mechanisms contributing to fatigue during RSE and does not constitute an endorsement or recommendation of any of the ergogenic
aids discussed.
2.9.3.1
Creatine
As repeated sprints produce a severe reduction in intramuscular
PCr concentration (Figure 2.9.4), it has been proposed that
increasing muscle PCr stores may improve RSA via a reduced
ATP degradation and a faster resynthesis of PCr between
sprints (Yquel et al., 2002). However, while creatine supplementation (typically ∼ 20 g/day for 5–7 days) has been reported
to improve intermittent-sprint performance (Preen et al., 2001;
Skare, Skadberg and Wisnes, 2001; van Loon et al., 2003;
Wiroth et al., 2001), it has not generally been reported to
improve repeated-sprint performance (Cornish, Chilibeck and
Burke, 2006; Delecluse, Diels and Goris, 2003; Glaister et al.,
2006; Kinugasa et al., 2004; McKenna et al., 1999). For
example, creatine supplementation (∼ 20 g/day for 5 days) has
been reported to improve the performance of repeated 10second cycle sprints interspersed with 60 seconds of recovery
(Wiroth et al., 2001), but not with 30 seconds of recovery
(Cornish, Chilibeck and Burke, 2006). More tellingly, within
one study, creatine supplementation was reported to improve
the performance of repeated six-second cycle sprints with
recovery intervals of 54 or 84 seconds, but not 24 seconds
(Preen et al., 2001). A possible explanation for these conflicting
findings is the proposal that creatine supplementation improves
intermittent-sprint performance via a faster resynthesis of PCr
between sprints (Yquel et al., 2002). Indeed, improved
intermittent-sprint performance has been associated with an
improved PCr replenishment rate (Preen et al., 2001). However,
as creatine supplementation has been reported to increase PCr
resynthesis after 60 and 120 seconds, but not 20 seconds
(Greenhaff et al., 1994) (Figure 2.9.7), this may explain why
creatine supplementation generally does not improve repeatedsprint performance (i.e. repeated sprints with recovery periods
of ∼30 seconds or less).
2.9.3.2
Carbohydrates
As the body’s carbohydrate stores are limited, it has been suggested that maintaining muscle glycogen stores could poten-
c17.indd 230
100
PCr content (mmol/kg dw)
230
90
Creatine
80
Placebo
*
*
70
60
50
40
30
20
10
0
Rest
Post Ex "+ 20 s" "+ 60 s""+ 120 s""+ 180 s"
Figure 2.9.7 Changes in resting and post-exercise PCr content
following short-term creatine supplementation (20 g/day for five
days); * P < 0.05 (Greenhaff et al., 1994; Preen et al., 2001)
H+
+
HCO3(Weak base)
H2CO3
(Weak acid)
H2O + CO2
Exhaled
Figure 2.9.8 The bicarbonate buffer system is present in both the
intracellular and extracellular fluids and operates to resist changes in
H+ concentration when a strong acid or base is added. When a strong
acid is added to the fluid, the bicarbonate ions ( HCO3− ) act as weak
bases to tie up the H+ released by the stronger acid, forming carbonic
acid (H2CO3). The [HCO3− ] in the extracellular fluid is normally
around 25 mmol/l at rest, and this has been reported to increase by an
average of 5.3 mmol/l after the ingestion 0.3 g/kg of body mass of
sodium bicarbonate (NaHCO3)
tially be important in attenuating fatigue during prolonged,
multiple-sprint exercise (Balsom et al., 1999). However, while
many studies have demonstrated that carbohydrate ingestion is
ergogenic for the performance of prolonged endurance exercise
(for review see Coggan and Coyle, 1991), there is limited
research that has investigated the effects of carbohydrate ingestion on repeated-sprint performance. In one of the few studies
to date, it was reported that increasing muscle glycogen stores
resulted in better maintenance of power output over 15 sixsecond sprints (with 30 seconds of rest between sprints) (Balsom
et al., 1999). These results suggest that carbohydrate loading
(e.g. 8–10 grams of carbohydrate per kilogram body mass over
the 24-hour period preceding exercise) can improve RSA.
2.9.3.3 Alkalizing agents
The ingestion of alkalizing agents (e.g. NaHCO3) prior to RSE
should improve performance by enhancing the efflux of H+
from the muscle into the blood, and thus maintaining muscle
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CHAPTER 2.9
REPEATED-SPRINT ABILITY (RSA)
231
13
80
Peak Power (W.kg -1)
*
*
12
*
11.5
11
10.5
Muscle lactate (mmol/kg dw)
12.5
70
Placebo
*
Sodium bicarbonate
60
50
40
30
20
10
0
10
1
2
3
Sprint Number
4
5
Pre
Post
Figure 2.9.9 (a) Peak power output during a five × six-second repeated-sprint exercise (RSE), following the ingestion of either sodium
bicarbonate or a placebo (NaCl). (b) Muscle lactate values before and after the RSE. Values are mean ± SE (N = 10). * denotes significant
difference from placebo (P < 0.05) (Bishop et al., 2004)
pH levels closer to normal during RSE (Hirche et al., 1976;
Mainwood and Worseley-Brown, 1975). Although the ergogenic benefits of alkaline ingestion have been largely attributed
to an enhanced extracellular buffer capacity, it has recently been
demonstrated that the ingestion of alkalizing agents (either
sodium bicarbonate or sodium citrate) can also reduce the
exercise-induced increase in extracellular K+ (Sostaric et al.,
2006; Street et al., 2005).
Many studies have investigated the effects of alkaline ingestion on high-intensity exercise performance (McNaughton,
Ford and Newbold, 1997; Spriet et al., 1986; Stephens et al.,
2002). There is however a paucity of studies that have investigated the effects of alkaline ingestion on RSA. Bishop et al.
(2004) reported a better power maintenance during sprints 3,
4, and 5 of a repeated-sprint test (five six-second sprints performed every 30 seconds) following the ingestion of 0.3 g/kg
of NaHCO3 (Figure 2.9.9). In support of this finding, Lavender
and Bird (1989) also reported NaHCO3 ingestion to be ergogenic for the performance of ten 10-second cycle sprints with
50 seconds of recovery in between. In contrast, NaHCO3 ingestion produced only a small (∼2%), non-significant improvement
in the performance of ten six-second running sprints (on a
non-motorized treadmill), separated by 30-second recovery
periods (Gaitanos et al., 1991). While it is possible that these
contrasting findings are due to differing effects of NaHCO3
ingestion on running and cycling repeated-sprint performance,
the more likely explanation is the relatively small change in
blood pH reported in the final study (7.38–7.43, possibly due
to the greater time delay (150 min) between ingestion and exercise). Thus, while confirmatory research is required, it appears
that alkaline ingestion (e.g. 0.3 g/kg of NaHCO3 90 minutes
before exercise), leading to a large increase in pH (∼0.1 of a
pH unit) and [HCO3− ] (∼5.0 mmol/l), is likely to improve
repeated-sprint performance. Furthermore, while improved K+
c17.indd 231
regulation may contribute to the improved performance, the
greater production of lactate suggests that reduced inhibition
of anaerobic glycolysis also plays a role (Figure 2.9.9). Such
studies suggest that H+ accumulation is indeed a limiting factor
during RSE.
2.9.3.4 Caffeine
Caffeine (1,3,7-trimethylxanthine) is the most commonly consumed drug in the world and is found in coffee, tea, cola,
chocolate, and various ‘energy’ drinks. While there is good
evidence that caffeine is also a potent ergogenic aid for many
athletic pursuits (Billaut and Basset, 2007; Billaut, Basset and
Falgairette, 2005), it is of limited value in providing better
understanding of the mechanisms contributing to fatigue during
RSE. This is because the ergogenic effects of caffeine have
been attributed to a number of possible mechanisms, including:
the blocking of adenosine receptors (Fredholm et al., 1999),
central nervous system facilitation (Williams, 1991), increased
Na+/K+ATPase activity (Lindinger, Graham and Spriet, 1993),
mobilization of intracellular calcium (Sinclair and Geiger,
2000), and increased plasma catecholamine concentration
(Mazzeo, 1991).
Nonetheless, research has investigated the effects of caffeine
(6 mg/kg of body mass) on multiple-sprint performance. Stuart
et al. (2005) reported a negligible effect of caffeine ingestion
on RSA (10 × 20-minute sprints performed every 10 seconds),
while Schneiker et al. (2006) reported a 7% increase in mean
power when 10 male team-sport athletes performed an
intermittent-sprint test consisting of two 36-minute ‘halves’,
each half comprising 18 four-second sprints with two minutes
of active recovery at 35% VO2peak between each sprint. Thus,
while further research is certainly warranted, these results
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PHYSIOLOGICAL ADAPTATIONS TO STRENGTH AND CONDITIONING
suggest that caffeine ingestion is likely to improve intermittent,
but not repeated, sprint performance.
2.9.3.5
2.9.4
EFFECTS OF TRAINING ON RSA
2.9.4.1
Introduction
Recently, there has been an increase in scientific research
regarding the importance of RSA for team- and racket-sport
athletes (Bravo et al., 2008; Girard et al., 2007; Impellizzeri
et al., 2008; Rampinini et al., 2007; Spencer et al., 2004, 2005).
Surprisingly, however, there has been little research about the
best training methods to improve this component. In the absence
of strong scientific evidence, one concept that has emerged is
the need to train RSA by performing RSE. While such a concept
appeals to common sense, the scientific evidence in support of
this approach is lacking. In this section, it will be argued that
the best way to improve RSA is to improve the underlying
factors responsible for fatigue (see Section 2.9.2).
Training the limiting factors
Ion regulation
The removal of H+ during intense skeletal muscle contractions
(such as repeated sprints) occurs via intracellular buffering
(βmin vitro) and a number of different membrane transport
systems, especially the monocarboxylate transporters (MCTs)
(Juel, 1998) (Figure 2.9.10). The muscle membrane also contains Na+–K+ pumps, which are largely responsible for the
maintenance of extracellular [K+] (Clausen, 2003).
A large increase in muscle H+ and/or lactate during exercise
has been proposed to be an important stimulus for adaptations
of the muscle pH-regulating systems (Weston et al., 1997).
This is supported by increases in βmin vitro in response to
high-intensity, but not moderate-intensity, endurance training
(Edge, Bishop and Goodman, 2006). However, greater accu-
c17.indd 232
H+
Summary
To date, few studies have investigated the effects of ergogenic
aids on RSA, and contradictory findings have often been
reported (possibly due to the effects of task dependency on
fatigue). Further research is required as such studies provide
important insights into possible determinants of fatigue during
RSE. For example, reports of improved repeated-sprint performance following alkaline ingestion provide support for the
hypothesis that H+ accumulation is an important limiting factor
during RSA. Similarly, decreases in RSA following the lowering of muscle glycogen stores suggest that, under certain
conditions, muscle glycogen content can limit RSA. While
creatine-loading studies do not support the hypothesis that PCr
availability is an impo